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Long-Lasting, Context-Dependent Modification of Stepping in the Cat After Repeated Stumbling-Corrective Responses
Abstract
A consistent feature of animal locomotion is the capacity to maintain stable movements in changing environments. Here we describe long-term modification of the swing movement of the hind leg in cats in response to repeatedly impeding the movement of the leg. While studying phase transitions in the hind legs, we discovered that repetitively evoking the stumbling-corrective reaction led to long-lasting increases in knee flexion and step height during swing to avoid the impediment. These increases were apparent after nearly 20 stimuli and maximal after about 120 stimuli and, in some animals, they persisted for > or =24 h after presentation of the stimuli. Furthermore, these long-lasting changes were context dependent and did not generalize to other environments; when walking was observed in an environment distinct from that used in training, the hind-limb kinematics returned to normal. To gain insight into what regions of the nervous system might be involved in this long-term modification, we examined the changes in stepping in decerebrate cats after multiple perturbed steps. In this situation, there was a short-term increase in step height, although this increase was smaller than that evoked in intact animals and persisted for <1 min after termination of the stimuli. Thus induction of the long-term increase in step height requires the forebrain. We propose that the conditioned change in leg movement is related to a general ability of animals to adapt locomotor movements to new features of the environment.
... For example, an unexpected obstacle intercepting the normal path of the foot without visual perception requires the central nervous system (CNS) to respond with a 'stumbling corrective reaction/ response' (SCR) (Forssberg et al., 1975(Forssberg et al., , 1977Prochazka et al., 1978;Forssberg, 1979). Although SCR has been described in detail using the cat as the animal model (Quevedo et al., 2005a,b;McVea and Pearson, 2007) as well as in humans (Potocanac et al., 2016), information regarding the spinal circuits mediating this reflex remain obscure. This is at least in part due to a lack of SCR studies in genetically tractable animal models, such as the mouse. ...
... Both stimulations were sufficient to modify the swing movement, consistent with the SCR. Furthermore, the EMG activation patterns of muscles during SCR in mice were similar to the pattern previously described in cats (Forssberg, 1979;Wand et al., 1980;McVea and Pearson, 2007), where increased flexor muscle activation lifted the leg over the rod. In addition, when the electrical stimulation of the saphenous nerve was delivered during stance phase, activation of the flexor muscle was absent, congruent with the cat experiments (Forssberg, 1979). ...
... Mechanical stimulation leaves open the question of whether a functional SCR can be elicited by only cutaneous afferent signals, as suggested from experiments in cats (Forssberg, 1979). Alternatively, proprioceptive feedback that signals changes in the natural angular joint movement due to obstacle contact (McVea and Pearson, 2007) could also contribute to the initiation of the SCR. To differentiate between these two possibilities, we recorded the SCR initiated by cutaneous afferent activation by electrical stimulation of the saphenous nerve that would mimic obstacle contact. ...
The ability to walk around in a natural environment requires the capacity to cope with unexpected obstacles that may disrupt locomotion. One such mechanism is called the stumbling corrective reaction (SCR) that enables animals to step over obstacles that would otherwise disturb the progression of swing movement. Here we use in vivo motion analysis and physiological recording techniques to describe the SCR in mice. We show that SCR can be elicited consistently in mice during locomotion by inserting an obstacle along the path of leg movement during swing phase. Furthermore, we show that the same behavior can be elicited if the saphenous nerve, a cutaneous nerve that would detect contact of the leg with an object, is stimulated electrically. This suggests that cutaneous afferent feedback is sufficient to elicit SCR. We further show that the SCR is phase dependent occurring only with stimulation during swing phase, but not during early stance. During SCR elicited by either method, the foot is lifted higher to clear the object by flexing the knee, via the semitendinosus muscle, and ankle joint, by tibialis anterior contraction. The latter also exhibits a brief extension before flexion onset. Our data provide a detailed description of SCR in mice and will be crucial for future research that aims to identify the interneurons of the premotor network controlling SCR and its neuronal mechanisms by combining motion analysis, electrophysiology, and mouse genetics.
... 1 3 be remarkably sensitive to changes in movement space (McVea and Pearson 2007;Reisman et al. 2009), direction (Krakauer et al. 2000;Hwang et al. 2006;Choi and Bastian 2007;Taylor and Ivry 2013), speed (Kitazawa et al. 1997;McVea and Pearson 2007;Francis 2008;, among other changes in motor and sensory context (e.g., Shelhamer and Clendaniel 2002;Reynolds and Bronstein 2004;Blau et al. 2009). ...
... 1 3 be remarkably sensitive to changes in movement space (McVea and Pearson 2007;Reisman et al. 2009), direction (Krakauer et al. 2000;Hwang et al. 2006;Choi and Bastian 2007;Taylor and Ivry 2013), speed (Kitazawa et al. 1997;McVea and Pearson 2007;Francis 2008;, among other changes in motor and sensory context (e.g., Shelhamer and Clendaniel 2002;Reynolds and Bronstein 2004;Blau et al. 2009). ...
... Tripping aftereffects in cats were also sensitive to changes in the walking environment. Aftereffects were absent when cats walked in a different environment (either an overground walkway or a walkway with spaced pegs to step on), and they re-emerged when the cats were returned to the treadmill (McVea and Pearson 2007). The speed of the over-ground walkway trials was not reported, so it was not clear whether walking speed contributed to the diminution of over-ground aftereffects. ...
Movements learned in one set of conditions may not generalize to other conditions. For example, practicing walking on a split-belt treadmill subsequently changes coordination between the legs during normal (“tied-belt”) treadmill walking; however, there is limited generalization of these aftereffects to natural walking over the ground. We hypothesized that generalization of split-belt treadmill adaptation to over-ground walking would be improved by maintaining consistency in other task variables, specifically gait speed. This hypothesis was based on our previous finding that treadmill aftereffect size was sensitive to gait speed: Aftereffects were largest when tested on tied-belts running at the same speed as the slower belt during split-belt adaptation. In the present study, healthy adults were assigned to a “slow” or “fast” over-ground walking group. Both groups adapted to split-belts (0.7:1.4 m/s), and treadmill aftereffects were tested on tied-belts at the slow (0.7 m/s) and fast (1.4 m/s) speeds. All participants were subsequently transferred to the over-ground environment. The slow and fast groups walked over-ground at 0.7 and 1.4 m/s, respectively. As in previous work, we found that the size of aftereffects during treadmill walking was speed-dependent, with larger aftereffects occurring at 0.7 m/s compared with 1.4 m/s. However, over-ground walking aftereffects were less sensitive to changes in gait speed. We also found that aftereffects in spatial coordination generalized more to over-ground walking than aftereffects in temporal coordination across all speeds of walking. This suggests that different factors influence aftereffect size in different walking environments and for different measures of coordination.
... There, however, has been no systematic examination as to whether there are residual effects manifested in subsequent step cycles in complete spinal animals. McVea and Pearson (2007) reported an elevated height of the swing phase after 20 or more consecutive perturbations of the swing phase in normal cats. This change in swing trajectory persisted up to 24 h and the magnitude of this effect generally reached a plateau within 120 repetitions of the perturbation. ...
... From a more highly integrative and conceptual perspective, these responses reflect "recognition" of a specific complex afferent pattern induced by the stimulus that results in an adjustment to a subsequent encounter within the time frame of a single step cycle, i.e., within the same step cycle the trajectory of the paw is changed in a way that tends to avoid the previous perturbation (Figures 1-4). The neuromotor strategy that mediates this ipsilateral hyperflexion during the swing phase after the tripping stimulus seems to be rather consistent for different experimental preparations ranging from intact locomotion to fictive locomotion (Quevedo et al., 2005;McVea and Pearson, 2007). A common feature of this response is an increase in step height and earlier initiation of activation, particularly of motor pools associated with knee flexion. ...
... These latter responses are highly coordinated responses requiring larger scale circuitries to control those motor pools that generate locomotion. Early and late responses to Frontiers in Physiology | Integrative Physiology stumbling perturbations that can sustain successful stepping after a stumble during locomotion have been observed in uninjured human adults (Schillings et al., 2000) and infants (Pang et al., 2003), decerebrated ferrets (Lou and Bloedel, 1988), intact cats (McVea and Pearson, 2007), and chronic spinal cats (Forssberg et al., 1975). Other more complex perturbations, such as applying force fields at specific phases of the step cycle in spinal rats, also demonstrate that there is a range of highly coordinated and immediate as well as delayed motor responses that have memory-related properties Heng and de Leon, 2007). ...
Adult cats with a complete spinal cord transection at T12–T13 can relearn over a period of days-to-weeks how to generate full weight-bearing stepping on a treadmill or standing ability if trained specifically for that task. In the present study, we assessed short-term (milliseconds to minutes) adaptations by repetitively imposing a mechanical perturbation on the hindlimb of chronic spinal cats by placing a rod in the path of the leg during the swing phase to trigger a tripping response. The kinematics and EMG were recorded during control (10 steps), trip (1–60 steps with various patterns), and then release (without any tripping stimulus, 10–20 steps) sequences. Our data show that the muscle activation patterns and kinematics of the hindlimb in the step cycle immediately following the initial trip (mechanosensory stimulation of the dorsal surface of the paw) was modified in a way that increased the probability of avoiding the obstacle in the subsequent step. This indicates that the spinal sensorimotor circuitry reprogrammed the trajectory of the swing following a perturbation prior to the initiation of the swing phase of the subsequent step, in effect “attempting” to avoid the re-occurrence of the perturbation. The average height of the release steps was elevated compared to control regardless of the pattern and the length of the trip sequences. In addition, the average impact force on the tripping rod tended to be lower with repeated exposure to the tripping stimulus. EMG recordings suggest that the semitendinosus, a primary knee flexor, was a major contributor to the adaptive tripping response. These results demonstrate that the lumbosacral locomotor circuitry can modulate the activation patterns of the hindlimb motor pools within the time frame of single step in a manner that tends to minimize repeated perturbations. Furthermore, these adaptations remained evident for a number of steps after removal of the mechanosensory stimulation.
... When an unanticipated obstacle with no pre-ceding visual cue is encountered, changes in limb trajectory can occur as result of paw contact with the obstacle. Limb trajectory changes initiated by stimuli directly to the surface of the paw or hindlimb are referred to as the stumbling corrective response (Forssberg, 1979;McVea and Pearson, 2007;Schillings et al., 1996). In contrast to the voluntary response, work in the low spinally transected cat indicates that this response can be mediated by spinal circuitry (Forssberg et al., 1975). ...
... This response caused hypermetric knee, and sometimes ankle, flexion after obstacle contact (compare Fig. 2F and G; 2H and I). The observed hypermetric flexion of the knee is in agreement with electromyograph (EMG) recordings by others that show activation of knee flexors after stimulation of the dorsal paw (Buford and Smith, 1993;Forssberg et al., 1977 ;McVea and Pearson, 2007). ...
... However, in the current study, recovery of a stumbling corrective response was seen beginning * 4 weeks post-injury. Although the exact amount of force was not measured, the observed limb displacement that occurred prior to eliciting the stumbling corrective response far exceeded contact (Forssberg, 1979;McVea and Pearson, 2007). Prochazka and colleagues (1978) suggest that the stumbling corrective response has an underlying proprioceptive stretch reflex in the ankle flexors, which surfaces when cutaneous sensory input to the dorsum of the paw is blocked. ...
Following a lateralized spinal cord injury (SCI) in humans, substantial walking recovery occurs; however, deficits persist in adaptive features of locomotion critical for community ambulation, including obstacle negotiation. Normal obstacle negotiation is accomplished by an increase in flexion during swing. If an object is unanticipated or supraspinal input is absent, obstacle negotiation may involve the spinally organized stumbling corrective response. How these voluntary and reflex components are affected following partial SCI is not well studied. This study is the first to characterize recovery of obstacle negotiation following low-thoracic spinal hemisection in the cat. Cats were trained pre- and post-injury to cross a runway with an obstacle. Assessments focused on the hindlimb ipsilateral to the lesion. Pre-injury, cats efficiently cleared an obstacle by increasing knee flexion during swing. Post-injury, obstacle clearance permanently changed. At 2 weeks, when basic overground walking ability been recovered, the hindlimb was dragged over the obstacle (∼90%). Surprisingly, the stumbling corrective response was not elicited until after 2 weeks. Despite a notable increase, between 4 and 8 weeks, in the ability to modify limb trajectory when approaching an obstacle, limb lift during obstacle approach was insufficient during ∼50% of encounters and continued to evoke the stumbling corrective response even at 16 weeks. A post-injury lead limb bias identified during negotiations with complete clearance, suggests a potential training strategy to increase the number of successful clearances. Therefore, following complete severing of half of the spinal cord, the ability to modify ipsilateral hindlimb trajectory shows significant recovery and by 16 weeks permits effective clearing of an obstacle, without contact, ∼50% of the time. Although this suggests plasticity of supporting circuitry, it is insufficient to support consistent clearance. This inconsistency, even at the most chronic time point assessed (16 weeks), is probably a contributing factor to falls reported for people with SCI.
... Skilled human walking requires not only tight regulation of intra-and interlimb coordination but also substantial flexibility to accommodate changes in physiologic conditions, environmental contexts, and behavioral goals. The neural control for such flexibility of coordination has been studied extensively in both animal and human models (Dietz et al. 1994;Forssberg et al. 1975Forssberg et al. , 1980Karayannidou et al. 2009;Lam et al. 2006;McVea and Pearson 2007;Pang et al. 2003;Pearson 2000Pearson , 2004. This research has shown that both feedback and feedforward mechanisms play an important role in modifying locomotion. ...
... This research has shown that both feedback and feedforward mechanisms play an important role in modifying locomotion. Feedback control can produce essential corrections to the locomotor pattern (Eng et al. 1994;Forssberg et al. 1975;Hiebert et al. 1994), whereas feedforward control affords the locomotor system the capability for making predictions (McVea and Pearson 2007;Morton and Bastian 2006). This is accomplished through stored knowledge of the body's dynamics and the external environment, which is used to estimate the appropriate neural commands for a given desired walking behavior (Blanchette and Bouyer 2009;McVea and Pearson 2007). ...
... Feedback control can produce essential corrections to the locomotor pattern (Eng et al. 1994;Forssberg et al. 1975;Hiebert et al. 1994), whereas feedforward control affords the locomotor system the capability for making predictions (McVea and Pearson 2007;Morton and Bastian 2006). This is accomplished through stored knowledge of the body's dynamics and the external environment, which is used to estimate the appropriate neural commands for a given desired walking behavior (Blanchette and Bouyer 2009;McVea and Pearson 2007). ...
Human walking must be flexible enough to accommodate many contexts and goals. One form of this flexibility is locomotor adaptation: a practice-dependent alteration to walking occurring in response to some novel perturbing stimulus. Although studies have examined locomotor adaptation and its storage by the CNS in humans, it remains unclear whether altered movements occurring in the leg contralateral to a perturbation are caused by true practice-dependent adaptation or whether they are generated via feedback corrective mechanisms. To test this, we recorded leg kinematics and electromyography (EMG) from nondisabled adults as they walked on a treadmill before, during, and after a novel force was applied to one leg, which resisted its forward movement during swing phase. The perturbation produced kinematic changes to numerous walking parameters, including swing phase durations, step lengths, and hip angular excursions. Nearly all occurred bilaterally. Importantly, kinematic changes were gradually adjusted over a period of exposure to the perturbation and were associated with negative aftereffects on its removal, suggesting they were adjusted through a true motor adaptation process. In addition, increases in the EMG of both legs persisted even after the perturbation was removed, providing further evidence that the CNS made and stored changes to feedforward motor commands controlling each leg. Our results show evidence for a feedforward adaptation of walking involving the leg opposite a perturbation. This result may help support the application of locomotor adaptation paradigms in clinical rehabilitation interventions targeting recovery of symmetric walking patterns in a variety of patient populations.
... Beyond lesioning studies, other work has also shown that subcortical centers participate heavily in the development of stimulus association and memory trace formation. Specifically, the work of McVea and Pearson (2007) corroborates much of what we have found regarding the carryover effect to further support the possible influence of subcortical centers in potentiating stimulusresponse associations and memory trace retention. Using a feline model, McVea and Pearson (2007) showed that after as few as 20 perturbations to the rear limb while walking on a treadmill, the modification to the cat's step height that was evoked by the perturbation persisted even when the impediment to normal walking was removed. ...
... Specifically, the work of McVea and Pearson (2007) corroborates much of what we have found regarding the carryover effect to further support the possible influence of subcortical centers in potentiating stimulusresponse associations and memory trace retention. Using a feline model, McVea and Pearson (2007) showed that after as few as 20 perturbations to the rear limb while walking on a treadmill, the modification to the cat's step height that was evoked by the perturbation persisted even when the impediment to normal walking was removed. They also observed that this step-height modification carried over to subsequent trials performed 20 min and up to 24 h post-conditioning. ...
... Like McVea and Pearson (2007), we used a similar number of perturbations to upright stance and were able to elicit carryover responses approximately 15 min after the initial conditioning procedure. Although McVea and Pearson (2007) argue that their paradigm was only "superficially" similar to classical conditioning because it did not employ the explicit use of a CS (such as an auditory cue), they suggest that the contextual specificity observed in the carryover responses implies the involvement of forebrain centers in memory trace retention (McVea and Pearson, 2007). In the current investigation, the EMG responses evoked in Cue-Only trials caused context-specific angular displacements of the shank that were consistently in the opposite direction to the displacements caused by the balance perturbation. ...
The purpose of the study was to determine whether the central nervous system (CNS) requires the sensory feedback generated by balance perturbations in order to trigger postural responses (PRs). In Experiment 1, twenty-one participants experienced toes-up support-surface tilts in two blocks. Control blocks involved unexpected balance perturbations whereas an auditory tone cued the onset of balance perturbations in Conditioning blocks. A single Cue-Only trial followed each block (Cue-Only(Control) and Cue-Only(Conditioning) trials) in the absence of balance perturbations. Cue-Only(Conditioning) trials were used to determine whether postural perturbations were required in order to trigger PRs. Counter-balancing the order of Control and Conditioning blocks allowed Cue-Only(Control) trials to examine both the audio-spinal/acoustic startle effects of the auditory cue and the carryover effects of the initial conditioning procedure. In Experiment 2, six participants first experienced five consecutive Tone-Only trials that were followed by twenty-five conditioning trials. After conditioning, five Tone-Only trials were again presented consecutively to first elicit and then extinguish the conditioned PRs. Surface electromyography (EMG) recorded muscle activity in soleus (SOL), tibialis anterior (TA) and rectus femoris (RF). EMG onset latencies and amplitudes were calculated together with the onset latency, peak and time-to-peak of shank angular accelerations. Results indicated that an auditory cue could be conditioned to initiate PRs in multiple muscles without balance-relevant sensory triggers generated by balance perturbations. Postural synergies involving excitation of TA and RF and inhibition of SOL were observed following the Cue-Only(Conditioning) trials that resulted in shank angular accelerations in the direction required to counter the expected toes-up tilt. Postural synergies were triggered in response to the auditory cue even 15 min post-conditioning. Furthermore, conditioned PRs were quickly extinguished as participants became unresponsive by the third trial in extinction. In conclusion, our results reveal that the CNS does not require sensory feedback from postural perturbations in order to trigger PRs.
... For example, area 5 neurons that respond to passive joint manipulation are even more responsive during active movements, demonstrating an integration of both sensory and motor inputs [40]. Correspondingly, previous work has demonstrated that, in comparison to trials where the animal is delayed just before the forelegs have stepped over an obstacle, obstacle memory is more robust when the animal is delayed after foreleg clearance [10,41]. These studies suggest that efference copies of motor commands for elevated foreleg stepping, the resulting proprioceptive feedback, or both are important for WM-guided obstacle locomotion. ...
... When HH testing was conducted, a minimum of 10 of these trials were completed. Given the propensity for animals to develop a learned avoidance response to repeated foreleg obstacle contact [41], TOP trials were completed no more than 5 times throughout a single recording session. Thus the subset of units included in the TOP analysis was dependent on unit stability (see below) to ensure that a minimum of 10 TOP trials were included in the statistical analyses. ...
In complex environments, information about surrounding obstacles is stored in working memory (WM) and used to coordinate appropriate movements for avoidance. In quadrupeds, this WM system is particularly important for guiding hindleg stepping, as an animal can no longer see the obstacle underneath the body following foreleg clearance. Such obstacle WM involves the posterior parietal cortex (PPC), as deactivation of area 5 incurs WM deficits, precluding successful avoidance. However, the neural underpinnings of this involvement remain undefined. To reveal the neural substrates of this behavior, microelectrode arrays were implanted to record neuronal activity in area 5 during an obstacle WM task in cats. Early in the WM delay, neurons were modulated generally by obstacle presence or more specifically in relation to foreleg step height. Thus, information about the obstacle or about foreleg clearance can be retained in WM. In a separate set of neurons, this information was recalled later in the delay in order to plan subsequent hindleg stepping. Such early and late delay period signals were temporally bridged by neurons exhibiting obstacle-modulated activity sustained throughout the delay. These neurons represented a specialized subset of all recorded neurons, which maintained stable information coding across the WM delay. Ultimately, these various patterns of task-related modulation enable stable representations of obstacle-related information within the PPC to support successful WM-guided obstacle negotiation in the cat.
... In turn, corticospinal and rubrospinal tracts signal spinal motor circuits to activate muscles and alter limb trajectory (Beloozerova and Sirota, 1993;Widajewicz et al., 1994;Drew et al., 1996;Lavoie and Drew, 2002). Without anticipatory control, the foot dorsum contacts the obstacle and a reflex, triggered by cutaneous afferents, which modifies limb trajectory to step away from and over the obstacle to prevent stumbling, termed the stumbling corrective reaction (SCR) (Prochazka et al., 1978;Forssberg, 1979;Wand et al., 1980;Buford and Smith, 1993;Schillings et al., 1996Schillings et al., , 2000Zehr et al., 1997;Quevedo et al., 2005;McVea and Pearson, 2007a). The SCR occurs in low-thoracic spinal-transected cats, consistent with a spinal mechanism (Forssberg et al., 1974(Forssberg et al., , 1975. ...
Following incomplete spinal cord injury in animals, including humans, substantial locomotor recovery can occur. However, functional aspects of locomotion, such as negotiating obstacles remains challenging. We collected kinematic and electromyography data in ten adult cats (5 males, 5 females) before and at weeks 1-2 and 7-8 after a lateral mid-thoracic hemisection on the right side of the cord while they negotiated obstacles of three different heights. Intact cats always cleared obstacles without contact. At weeks 1-2 after hemisection, the ipsilesional right hindlimb contacted obstacles in ∼50% of trials, triggering a stumbling corrective reaction or absent responses, which we termed Other. When complete clearance occurred, we observed exaggerated ipsilesional hindlimb flexion when crossing the obstacle with contralesional left limbs leading. At weeks 7-8 after hemisection, the proportion of complete clearance increased, Other responses decreased, and stumbling corrective reactions remained relatively unchanged. We found redistribution of weight support after hemisection, with reduced diagonal supports and increased homolateral supports, particularly on the left contralesional side. The main neural strategy for complete clearance in intact cats consisted of increased knee flexor activation. After hemisection, ipsilesional knee flexor activation remained but it was insufficient or more variable as the limb approached the obstacle. Intact cats also increased their speed when stepping over an obstacle, an increase that disappeared after hemisection. The increase in complete clearance over time after hemisection paralleled the recovery of muscle activation patterns or new strategies. Our results suggest partial recovery of anticipatory control through neuroplastic changes in the locomotor control system.
Significance statement:
Most spinal cord injuries (SCI) are incomplete and people can recover some walking functions. However, the main challenge for people with SCI that do recover a high level of function is to produce a gait that can adjust to everyday occurrences, such as turning, stepping over an obstacle, etc. Here, we use the cat model to answer two basic questions: How does an animal negotiate an obstacle after an incomplete SCI and why does it fail to safely clear it? We show that the inability to clear an obstacle is because of improper activation of muscles that flex the knee. Animals recover a certain amount of function thanks to new strategies and changes within the nervous system.
... In lamprey and other undulatory animals, while generating a spatiotemporal pattern for propulsion, the motor circuits also precisely and contextually tune the body's biomechanical responses to the external conditions (Berri et al., 2009;Blight, 1977;Fang-Yen et al., 2010;Ji et al., 2021a;LONG, 1998;Tytell et al., 2018). Kinematic and electromyographic studies in legged animals characterized a phasic compensatory reaction in a perturbed animal, which induces rapid corrective movements adapted to the perturbation (Dietz et al., 1987;Forssberg, 1979;Forssberg et al., 1975Forssberg et al., , 1977Mayer and Akay, 2018;McVea and Pearson, 2007;Potocanac et al., 2016;Prochazka et al., 1978). ...
Neural circuits coordinate with muscles and sensory feedback to generate motor behaviors appropriate to its natural environment. Studying mechanisms underlying complex organism locomotion has been challenging, partly due to the complexity of their nervous systems. Here, I used the roundworm C. elegans to understand the locomotor circuit. With its well-mapped nervous system, easily-measurable movements, genetic manipulability, and many human homologous genes, C. elegans has been commonly used as a model organism for dissecting the circuit, cellular, and molecular principles of locomotion. My work introduces two separate approaches to probe the mechanisms by which the C. elegans motor circuit generates and modulates undulations. First, I quantified C. elegans movements during free locomotion and during transient muscle inhibition. Undulations were asymmetrical with respect to the duration of bending and unbending per cycle. Phase response curves induced by brief optogenetic head muscle inhibitions showed gradual increases and rapid decreases as a function of phase at which the perturbation was applied. A relaxation oscillator model was developed based on proprioceptive thresholds that switch the active muscle moment. It quantitatively agrees with data from free movement, phase responses, and previous results for gait adaptation to mechanical loads. Next, I characterized a proprioception-mediated compensatory behavior during C. elegans forward locomotion: the anterior body bending amplitude compensates for the change in midbody bending amplitude by an opposing homeostatic response. I demonstrated that curvature compensation requires dopamine signaling driven by PDE neurons. Calcium imaging experiments suggested a proprioceptive functionality for PDE in sensing midbody curvature. Downstream of PDE dopamine signaling, curvature compensation requires D2-like dopamine receptor DOP-3 in the interneurons AVK. FMRFamide-like neuropeptide FLP-1, released by AVK, regulates SMB motor neurons via receptor NPR-6 to modulate anterior bending amplitude. These results revealed a mechanism whereby proprioception works with dopamine and neuropeptide signaling to mediate homeostatic locomotor control. Together, through a consolidation of experimental and computational approaches, I found C. elegans utilizes its circuitry not only to act motor behaviors but to adjust/correct its ongoing behaviors in its natural contexts.
... **p , 0.01, ***p , 0.001. Mayer and Akay, 2018), or does proprioceptive feedback that signals changes in the natural angular joint movement because of obstacle contact (McVea and Pearson, 2007) also contribute to the initiation of the SCR? Our previous data suggested that cutaneous touch signaling is sufficient to elicit SCR (Mayer and Akay, 2018). ...
Safe and efficient locomotion relies on placing the foot on a reliable surface at the end of each leg swing movement. Visual information has been shown to be important for determining the location of foot placement in humans during walking when precision is required. Yet in quadrupedal animals where the hindlimbs are outside of the visual field, such as in mice, the mechanisms by which precise foot placement is achieved remain unclear. Here we show that the placement of the hindlimb paw is determined by the position of the forelimb paw during normal locomotion and in the presence of perturbations. When a perturbation elicits a stumbling corrective reaction, we found that the forelimb paw shifts posteriorly relative to body at the end of stance, and this spatial shift is echoed in hindlimb paw placement at the end of the swing movement. Using a mutant mouse line in which muscle spindle feedback is selectively removed, we show that this posterior shift of paw placement is dependent on muscle spindle feedback in the hindlimb but not in the forelimb. These findings uncover a neuronal mechanism that is independent of vision to ensure safe locomotion during perturbation. This mechanism adds to our general knowledge of how the nervous system controls targeted limb movements and could inform the development of autonomous walking machines.
... Unexpected sensory stimuli result in reflexive changes, and with repetition, adaptation to the sensory stimuli occurs. For example, if an obstacle is placed in front of a cat's hind-limb during the swing phase causing activation of cutaneous receptors on the dorsum of the paw, the knee will flex further to clear the obstacle (Mcvea and Pearson 2007). This is a reflexive, or automatic response to the sensory stimulus, which is mediated by the spinal cord. ...
Objective. Neuromodulation technologies are increasingly used for improving function after neural injury. To achieve a symbiotic relationship between device and user, the device must augment remaining function, and independently adapt to day-to-day changes in function. The goal of this study was to develop predictive control strategies to produce over-ground walking in a model of hemisection spinal cord injury (SCI) using intraspinal microstimulation (ISMS). Approach. Eight cats were anaesthetized and placed in a sling over a walkway. The residual function of a hemisection SCI was mimicked by manually moving one hind-limb through the walking cycle. ISMS targeted motor networks in the lumbosacral enlargement to activate muscles in the other, presumably ‘paralyzed’ limb, using low levels of current (<130 μA). Four people took turns to move the ‘intact’ limb, generating four different walking styles. Two control strategies, which used ground reaction force and angular velocity information about the manually moved ‘intact’ limb to control the timing of the transitions of the ‘paralyzed’ limb through the step cycle, were compared. The first strategy used thresholds on the raw sensor values to initiate transitions. The second strategy used reinforcement learning and Pavlovian control to learn predictions about the sensor values. Thresholds on the predictions were then used to initiate transitions. Main results. Both control strategies were able to produce alternating, over-ground walking. Transitions based on raw sensor values required manual tuning of thresholds for each person to produce walking, whereas Pavlovian control did not. Learning occurred quickly during walking: predictions of the sensor signals were learned rapidly, initiating correct transitions after ≤4 steps. Pavlovian control was resilient to different walking styles and different cats, and recovered from induced mistakes during walking. Significance. This work demonstrates, for the first time, that Pavlovian control can augment remaining function and facilitate personalized walking with minimal tuning requirements.
... Unexpected sensory stimuli result in reflexive changes, and with repetition, adaptation to the sensory stimuli occurs. For example, if an obstacle is placed in front of a cat's hind-limb during the swing phase causing activation of cutaneous receptors on the dorsum of the paw, the knee will flex further to clear the obstacle (McVea and Pearson 2007). This is a reflexive, or automatic response to the sensory stimulus, which is mediated by the spinal cord. ...
Objective: Neural interface technologies are more commonly used in people with neural injury. To achieve a symbiotic relationship between device and user, the control system of the device must augment remaining function and adapt to day-to-day changes. The goal of this study was to develop predictive control strategies to produce alternating, over-ground walking in a cat model of hemisection spinal cord injury (SCI) using intraspinal microstimulation (ISMS).
Approach: Eight cats were anaesthetized and placed in a sling over a walkway. The residual function of a hemisection SCI was mimicked by manually moving one hind-limb through the walking cycle over the walkway. ISMS targeted motor networks in the lumbosacral enlargement to activate muscles in the other limb using low levels of current (< 130 uA). Four different people took turns to move the "intact" limb. Two control strategies, which used ground reaction force and angular velocity information about the manually moved limb to control the timing of the transitions of the other limb, were compared. The first strategy, reaction-based control, used thresholds on the sensor values to initiate state transitions. The other strategy used a reinforcement learning strategy, Pavlovian control, to learn predictions about the sensor values. Thresholds on the predictions were used to initiate transitions.
Main Results: Both control strategies were able to produce alternating, over-ground walking. Reaction-based control required manual tuning of the thresholds for each person to produce walking, whereas Pavlovian control did not. We demonstrate that learning occurs quickly during walking. Predictions of the sensor signals were learned quickly, initiating transitions in no more than 4 steps. Pavlovian control was resilient to transitions between people walking the limb, between cat experiments, and recovered from mistakes during walking.
Significance: This work demonstrates that Pavlovian control can augment remaining function and allow for personalized walking with minimal tuning requirements.
... Some locomotor adaptation studies have shown minimal transfer to new environmental contexts or demands. 13,14 Reisman et al 8 found that both stroke and neurologically intact subjects demonstrated partial transfer of the aftereffects observed on the treadmill to overground walking following split-belt treadmill walking. However, it is noteworthy that transfer was only partial. ...
Background:
Studies in neurologically intact subjects suggest that the gradual presentation of small perturbations (errors) during learning results in better transfer of a newly learned walking pattern to overground walking. Whether the same result would be true after stroke is not known.
Objective:
To determine whether introducing gradual perturbations, during locomotor learning using a split-belt treadmill influences learning the novel walking pattern or transfer to overground walking poststroke.
Methods:
Twenty-six chronic stroke survivors participated and completed the following walking testing paradigm: baseline overground walking; baseline treadmill walking; split-belt treadmill/adaptation period (belts moving at different speeds); catch trial (belts at same speed); post overground walking. Subjects were randomly assigned to the Gradual group (gradual changes in treadmill belts speed during adaptation) or the Abrupt group (a single, large, abrupt change during adaptation). Step length asymmetry adaptation response on the treadmill and transfer of learning to overground walking was assessed.
Results:
Step length asymmetry during the catch trial was the same between groups ( P = .195) confirming that both groups learned a similar amount. The magnitude of transfer to overground walking was greater in the Gradual than in the Abrupt group ( P = .041).
Conclusions:
The introduction of gradual perturbations (small errors), compared with abrupt (larger errors), during a locomotor adaptation task seems to improve transfer of the newly learned walking pattern to overground walking poststroke. However, given the limited magnitude of transfer, future studies should examine other factors that could impact locomotor learning and transfer poststroke.
... Animals adjust their motions according to external conditions. Normally, perturbations such as forces opposing motion [1] or impediments blocking stride execution [2] cause animals to adapt to external conditions. When perturbations are unpredictable and uncontrollable, however, animals modify their behavior in a manner that does not necessarily help them to negotiate the perturbation [3]. ...
Exposure to unpredictable and uncontrollable conditions causes animals to perceive stress and change their behavior. It is unclear how the perception of stress modifies the motor components of behavior and which molecular pathways affect the behavioral change. In order to understand how stress affects motor function, we developed an experimental platform that quantifies walking motions in Drosophila. We found that stress induction using electrical shock results in backwards motions of the forelegs at the end of walking strides. These leg retrogressions persisted during repeated stimulation, although they habituated substantially. The motions also continued for several strides after the end of the shock, indicating that stress induces a behavioral aftereffect. Such aftereffect could also be induced by restricting the motion of the flies via wing suspension. Further, the long-term effects could be amplified by combining either immobilization or electric shock with additional stressors. Thus, retrogression is a lingering form of response to a broad range of stressful conditions, which cause the fly to search for a foothold when it faces extreme and unexpected challenges. Mutants in the cAMP signaling pathway enhanced the stress response, indicating that this pathway regulates the behavioral response to stress. Our findings identify the effect of stress on a specific motor component of behavior and define the role of cAMP signaling in this stress response.
... The authors speculated that the legs have access to the stored motor plan of the arms, but not vice versa. From an evolutionary perspective, the hindlimbs of quadrupedal forward walking mammals must encounter the same obstacles as the forelimbs do, but the same situation does not occur in the reverse (McVea and Pearson 2007) and this could explain the unidirectional transfer of stored motor plans reported in this study. The results of this study are in contrast to previous findings of the same authors during a similar paradigm. ...
... motor learning; motor adaptation; locomotion; walking; retention; human ONE IMPORTANT FEATURE OF LOCOMOTION is the ability to adjust the walking pattern in response to altered conditions. The central nervous system (CNS) achieves these adjustments through the use of both feedback (Forssberg et al. 1975) and feedforward (McVea and Pearson 2007; Reisman et al. 2005; Morton and Bastian 2006) control. Motor adaptation is one way in which locomotor patterns are modified in a feedforward manner, specifically in response to some novel or unexpected but predictable perturbation (Shadmehr and Mussa-Ivaldi 1994). ...
Motor adaptation in response to gradual versus abrupt perturbation schedules may involve different neural mechanisms, potentially leading to different levels of motor memory. However, no study has investigated whether perturbation schedules alter memory of a locomotor adaptation across days. We measured adaptation and retention (memory) of altered interlimb symmetry during walking in two groups of participants over two days. On day 1, participants adapted to either a single, large perturbation (abrupt schedule) or a series of small perturbations that increased in size over time (gradual schedule). Retention was examined on day 2. On day 1, initial swing time and foot placement symmetry error sizes differed between groups but overall adaptation magnitudes were similar. On day 2, participants in both groups showed similar retention, re-adaptation, and aftereffect sizes, although there were some trends for improved memory in the abrupt group. These results conflict with previous data but are consistent with newer studies reporting no behavioral differences following adaptation using abrupt versus gradual schedules. Although memory levels were very similar between groups, we cannot rule out the possibility that the neural mechanisms underlying this memory storage differ. Overall, it appears that adaptation of locomotor patterns via abrupt and gradual perturbation schedules produces similar expression of locomotor memories across days.
... These observations suggest that the flexibility of walking depends to some degree on learning different patterns of locomotion, each appropriate for a particular situation and used when needed. Recently, our laboratory has completed a series of experiments that provide evidence that supports this hypothesis (McVea and Pearson 2007). These experiments examined the modifications in the swing phase of a hind leg of walking cats in response to repetitive tactile stimuli of the dorsum of the paw. ...
Animals in their natural environments display a remarkably diverse variety of walking patterns. Although some of this diversity is generated by alterations in feedback from the moving limbs, animals can modify their walking in many ways that cannot be directly attributed to this sensory feedback. For example, animals and humans can learn to associate a particular environment with disturbances that were experienced there earlier, and alter their stepping accordingly even after the disturbance has ceased. Another relevant example is that walking animals are aware of the locations of obstacles around them, and use this awareness to alter their stepping patterns even when there is no visual information available about the location of the obstacles relative to the body. In this article, we discuss recent work from our laboratory that addresses these two topics. First, we report that perturbing walking cats in a consistent manner evokes long-lasting changes to the walking pattern that are expressed only in the context in which walking was disturbed. Secondly, we show that cats that have stepped over an obstacle remember the location of that obstacle relative to the body during long delays, and can use that memory to guide stepping. The general theme of this research is that sensory inputs that signal context-the visual and auditory environment that surrounds an animal-play an important role in shaping the basic pattern of locomotion.
... For instance, descending commands from the motor cortex in cats are responsible for changes in limb trajectory and accurate paw placement that is required for stepping over obstacles on the treadmill (Beloozerova et al. 1993; Armstrong et al. 1996; Kably et al. 1998). Another study by McVea in cats claimed the forebrain to be responsible for long-term (>24 hours) aftereffects developed after repetitive presentation of obstacles (McVea et al. 2007). The aftereffect was an increase in step height of the hind limb even when no obstacles were present. ...
This study characterized the brain electrical activity during pedaling, a locomotor-like task, in humans. We postulated that phasic brain activity would be associated with active pedaling, consistent with a cortical role in locomotor tasks. 64 channels of electroencephalogram (EEG) and 10 channels of electromyogram (EMG) data were recorded from 10 neurologically-intact volunteers while they performed active and passive (no effort) pedaling on a custom-designed stationary bicycle. Ensemble average waveforms, two dimensional topographic maps and amplitude of the beta (13-35 Hz) frequency band were analyzed and compared between active and passive trials. The absolute amplitude (peak positive-peak negative) of the EEG waveform recorded at the Cz electrode tended to be higher in the passive than the active trials (paired t-test; p<0.01). Average power of the center beta-band frequency (20-25 Hz) in the active pedaling was significantly smaller than passive pedaling (Univariate ANOVA; p<0.01), consistent with beta desynchronization. A significant negative correlation was observed between the ensemble average EEG waveform for active trials and the composite EMG (summated EMG from both limbs for each muscle) of the rectus femoris (r = -0.77, p<0.01) the medial hamstrings (r = -0.85, p<0.01) and the tibialis anterior (r = -0.70, p <0.01) muscles. These results demonstrated that substantial sensorimotor processing occurs in the brain during pedaling in humans. Further, cortical activity seemed to be greatest during recruitment of the muscles critical for transitioning the legs from flexion to extension and vice versa. This is the first known study demonstrating the feasibility of EEG recording during pedaling, and owing to similarities between pedaling and bipedal walking, may provide valuable insight into brain activity during locomotion in humans.
... 15 In agreement, a recent study of gait adaptation in cats which results in aftereffects similar to our paradigm, 16 including dependence on visual context, also suggests cortical involvement. 17 However, subcortical activity is also likely to be involved in the underlying motor adaptation process. Morton and Bastian 18 recently investigated this issue using the split-belt paradigm, in which subjects adapt their gait to a treadmill in which the two legs walk at different speeds. ...
Gait adaptation is crucial for coping with varying terrain and biological needs. It is also important that any acquired adaptation is expressed only in the appropriate context. Here we review a recent series of experiments that demonstrate inappropriate expression of gait adaptation. We show that a brief period of walking onto a platform previously experienced as moving results in a large forward sway aftereffect, despite full awareness of the changing context. The adaptation mechanisms involved in this paradigm are extremely fast, just 1-2 discrete exposures to the moving platform result in the motor aftereffect. This aftereffect occurs even if subjects deliberately attempt to suppress it. However, it disappears when the location or method of gait is altered, indicating that aftereffect expression is context dependent. Conversely, making gait self-initiated increases sway during the aftereffect. This aftereffect demonstrates a profound dissociation between knowledge and action. The absence of generalization suggests a relatively simple form of motor learning, albeit involving high-level processing by cortical and cerebellar structures.
Following incomplete spinal cord injury in animals, including humans, substantial locomotor recovery can occur. However, functional aspects of locomotion, such as negotiating an obstacle remains challenging. We collected kinematic and electromyography data in ten adult cats before and at weeks 1-2 and 7-8 after a lateral mid-thoracic hemisection while they negotiated obstacles of three different heights. Intact cats always cleared obstacles without contact. At weeks 1-2 after hemisection, the ipsilesional hindlimb contacted obstacles in ~50% of trials, triggering a stumbling corrective reaction or lack of response. When complete clearance occurred, we observed exaggerated ipsilesional hindlimb flexion when it crossed the obstacle with the contralesional limbs leading. At weeks 7-8 after hemisection, complete clearance increased in favor of absent responses while the proportion of stumbling corrective reactions remained relatively the same. We found redistribution of weight support after hemisection, with reduced diagonal supports and increased homolateral supports, particularly on the contralesional side. The main neural strategy for complete clearance in intact cats consisted of increased activation of muscles that flex the knee. After hemisection, knee flexor activation remained but it was insufficient or more variable as the limb approached the obstacle. Intact cats also increased their speed when stepping over an obstacle, an increase that disappeared after hemisection. The increase in complete clearance over time after hemisection paralleled the recovery of muscle activation patterns or new strategies. Our results suggest partial recovery of anticipatory control through neuroplastic changes in the locomotor control system.
Proprioceptive feedback from skeletal muscle is an integral element of motor control, yet the precise physiological roles of muscle spindle (MS) and Golgi tendon organ (GTO) sensory receptors have remained difficult to disentangle due to technical limitations. New insights into the molecular basis of MS and GTO afferent subtypes offers genetic opportunities to further our understanding of the distinct functional features of these proprioceptor classes, while at the same time revealing additional layers of complexity in the regulation of coordinated motor output.
Visual cues can be used to train walking patterns. Here, we studied the performance and learning capacities of healthy subjects executing a high-precision visuomotor walking task, in an augmented reality training set-up. A beamer was used to project visual stepping targets on the walking surface of an instrumented treadmill. Two speeds were used to manipulate task difficulty. All participants (n = 20) had to change their step length to hit visual stepping targets with a specific part of their foot, while walking on a treadmill over seven consecutive training blocks, each block composed of 100 stepping targets. Distance between stepping targets was varied between short, medium and long steps. Training blocks could either be composed of random stepping targets (no fixed sequence was present in the distance between the stepping targets) or sequenced stepping targets (repeating fixed sequence was present). Random training blocks were used to measure non-specific learning and sequenced training blocks were used to measure sequence-specific learning. Primary outcome measures were performance (% of correct hits), and learning effects (increase in performance over the training blocks: both sequence-specific and non-specific). Secondary outcome measures were the performance and stepping-error in relation to the step length (distance between stepping target). Subjects were able to score 76% and 54% at first try for lower speed (2.3 km/h) and higher speed (3.3 km/h) trials, respectively. Performance scores did not increase over the course of the trials, nor did the subjects show the ability to learn a sequenced walking task. Subjects were better able to hit targets while increasing their step length, compared to shortening it. In conclusion, augmented reality training by use of the current set-up was intuitive for the user. Suboptimal feedback presentation might have limited the learning effects of the subjects.
In complex environments, tripping over an unexpected obstacle evokes the stumbling corrective reaction, eliciting rapid limb hyperflexion to lift the leg over the obstruction. While stumbling correction has been characterized within a single limb in the cat, this response must extend to both forelegs and hindlegs for successful avoidance in naturalistic settings. Furthermore, the ability to remember an obstacle over which the forelegs have tripped is necessary for hindleg clearance if locomotion is delayed. Therefore, memory-guided stumbling correction was studied in walking cats after the forelegs tripped over an unexpected obstacle. Tactile input to only one foreleg was often sufficient in modulating stepping of all four legs when locomotion was continuous, or when hindleg clearance was delayed. When obstacle height was varied, animals appropriately scaled step height to obstacle height. As tactile input without foreleg clearance was insufficient in reliably modulating stepping, efference, or proprioceptive information about modulated foreleg stepping may be important for producing a robust, long-lasting memory. Finally, cooling-induced deactivation of parietal area 5 altered hindleg stepping in a manner indicating that animals no longer recalled the obstacle over which they had tripped. Altogether, these results demonstrate the integral role area 5 plays in memory-guided stumbling correction.
Walking is the most common terrestrial form of locomotion in animals. Its great versatility and flexibility has led to many attempts at building walking machines with similar capabilities. The control of walking is an active research area both in neurobiology and robotics, with a large and growing body of work. This paper gives an overview of the current knowledge on the control of legged locomotion in animals and machines and attempts to give walking control researchers from biology and robotics an overview of the current knowledge in both fields. We try to summarize the knowledge on the neurobiological basis of walking control in animals, emphasizing common principles seen in different species. In a section on walking robots, we review common approaches to walking controller design with a slight emphasis on biped walking control. We show where parallels between robotic and neurobiological walking controllers exist and how robotics and biology may benefit from each other. Finally, we discuss where research in the two fields diverges and suggest ways to bridge these gaps.
The cat can recover a robust pattern of hindlimb locomotion following partial or complete spinal cord injuries. As a result, it has been instrumental in our understanding of spinal networks controlling and regulating locomotor activity. Thanks to our feline friend, spinal cord-injured humans are now trained on a treadmill to promote the recovery of walking. This chapter highlights some of the landmark studies using the cat that have led to a better understanding of the adaptive changes that take place after spinal cord injury, as well as the underlying mechanisms governing locomotor control and recovery.
There is an increasing interest in conceiving robotic systems that are able to move and act in an unstructured and not predefined environment, for which autonomy and adaptability are crucial features. In nature, animals are autonomous biological systems, which often serve as bio-inspiration models, not only for their physical and mechanical properties, but also their control structures that enable adaptability and autonomy-for which learning is (at least) partially responsible. This work proposes a system which seeks to enable a quadruped robot to online learn to detect and to avoid stumbling on an obstacle in its path. The detection relies in a forward internal model that estimates the robot's perceptive information by exploring the locomotion repetitive nature. The system adapts the locomotion in order to place the robot optimally before attempting to step over the obstacle, avoiding any stumbling. Locomotion adaptation is achieved by changing control parameters of a central pattern generator (CPG)-based locomotion controller. The mechanism learns the necessary alterations to the stride length in order to adapt the locomotion by changing the required CPG parameter. Both learning tasks occur online and together define a sensorimotor map, which enables the robot to learn to step over the obstacle in its path. Simulation results show the feasibility of the proposed approach.
Determine whether adaptation to a swing phase perturbation during gait transferred from treadmill to overground walking, the rate of overground deadaptation, and whether overground aftereffects improved step length asymmetry in persons with hemiparetic stroke and gait asymmetry.
Ten participants with stroke and hemiparesis and 10 controls walked overground on an instrumented gait mat, adapted gait to a swing phase perturbation on a treadmill, then walked overground on the gait mat again. Outcome measures, primary: overground step length symmetry, rates of treadmill step length symmetry adaptation and overground step length symmetry deadaptation; secondary: overground gait velocity, stride length, and stride cycle duration.
Step length symmetry aftereffects generalized to overground walking and adapted at a similar rate on the treadmill in both groups. Aftereffects decayed at a slower rate overground in participants with stroke and temporarily improved overground step length asymmetry. Both groups' overground gait velocity increased post adaptation due to increased stride length and decreased stride duration.
Stroke and hemiparesis do not impair generalization of step length symmetry changes from adapted treadmill to overground walking, but prolong overground aftereffects.
Motor adaptation during treadmill walking may be an effective treatment for improving overground gait asymmetries post-stroke.
The aim of this study was to explore the neural basis of adaptation, memory and skill transfer during human stepping over obstacles. Whilst walking on a treadmill, subjects had to perform uni- and bilateral obstacle steps. Acoustic feedback information about foot clearance was provided. Non-noxious electrical stimuli were applied to the right tibial nerve during the mid-stance phase of the right leg, i.e. 'prior' to the right or 'during' the left leg swing over the obstacle. The electromyogram (EMG) responses evoked by these stimuli in arm and leg muscles are known to reflect the neural coordination during normal and obstacle steps. The leading and trailing legs rapidly adapted foot clearance during obstacle steps with small further changes when the same obstacle condition was repeated. This adaptation was associated with a corresponding decrease in arm and leg muscle reflex EMG responses. Arm (but not leg) muscle EMG responses were greater when the stimulus was applied 'during' obstacle crossing by the left leg leading compared with stimulation 'prior' to right leg swing over the obstacle. A corresponding difference existed in arm muscle background EMG. The results indicate that, firstly, the somatosensory information gained by the performance and adaptation of uni- and bilateral obstacle stepping becomes transferred to the trailing leg in a context-specific manner. Secondly, EMG activity in arm and leg muscles parallels biomechanical adaptation of foot clearance. Thirdly, a consistently high EMG activity in the arm muscles during swing over the obstacle is required for equilibrium control. Thus, such a precision locomotor task is achieved by a context-specific, coordinated activation of arm and leg muscles for performance and equilibrium control that includes adaptation, memory and skill transfer.
Posture and movements are our only physical means of interacting with the environment. As we express our thoughts and emotions through posture and movements, they indicate our will or intentions. Locomotion is representative of purposeful goal-directed behaviors that are initiated by signals arising from either volitional processing in the cerebral cortex or emotional processing in the limbic system. Regardless of whether the locomotion is volitional or emotional, it is accompanied by automatically controlled movement processes such as the adjustment of postural muscle tone and rhythmic limb movements that are unconsciously executed. Sensori-motor integration at the level of the brainstem and spinal cord plays major roles in this automatic control. Signals processed in the basal ganglia and the cerebellum act on the cerebral cortex, the limbic system and the brainstem so that locomotor behaviors are appropriately and precisely regulated depending on the behavioral context. The purpose of this review is to describe how purposeful locomotor behaviors are initiated, executed and regulated so as to enable locomotive subjects to interact with and adapt to the environment.
In this review, we have tried to elucidate substrates for the execution of normal gait and to understand pathophysiological mechanisms of gait failure in basal ganglia dysfunctions. In Parkinson’s disease, volitional and emotional expressions of movement processes are seriously affected in addition to the disturbance of automatic movement processes, such as adjustment of postural muscle tone before gait initiation and rhythmic limb movements during walking. These patients also suffer from muscle tone rigidity and postural instability, which may also cause reduced walking capabilities in adapting to various environments. Neurophysiological and clinical studies have suggested the importance of basal ganglia connections with the cerebral cortex and limbic system in the expression of volitional and emotional behaviors. Here we hypothesize a crucial role played by the basal ganglia-brainstem system in the integrative control of muscle tone and locomotion. The hypothetical model may provide a rational explanation for the role of the basal ganglia in the control of volitional and automatic aspects of movements. Moreover, it might also be beneficial for understanding pathophysiological mechanisms of basal ganglia movement disorders. A part of this hypothesis has been supported by studies utilizing a constructive simulation engineering technique that clearly shows that an appropriate level of postural muscle tone and proper acquisition and utilization of sensory information are essential to maintain adaptable bodily functions for the full execution of bipedal gait.
In conclusion, we suggest that the major substrates for supporting bipedal posture and executing bipedal gait are 1) fine neural networks such as the cortico-basal ganglia loop and basal ganglia-brainstem system, 2) fine musculoskeletal structures with adequately developed (postural) muscle tone, and 3) proper sensory processing. It follows that any dysfunction of the above sensorimotor integration processes would result in gait disturbance.
Here, we used an obstacle treadmill experiment to investigate the neuromuscular control of locomotion in uneven terrain. We measured in vivo function of two distal muscles of the guinea fowl, lateral gastrocnemius (LG) and digital flexor-IV (DF), during level running, and two uneven terrains, with 5 and 7 cm obstacles. Uneven terrain required one step onto an obstacle every four to five strides. We compared both perturbed and unperturbed strides in uneven terrain to level terrain. When the bird stepped onto an obstacle, the leg became crouched, both muscles acted at longer lengths and produced greater work, and body height increased. Muscle activation increased on obstacle strides in the LG, but not the DF, suggesting a greater reflex contribution to LG. In unperturbed strides in uneven terrain, swing pre-activation of DF increased by 5 per cent compared with level terrain, suggesting feed-forward tuning of leg impedance. Across conditions, the neuromechanical factors in work output differed between the two muscles, probably due to differences in muscle-tendon architecture. LG work depended primarily on fascicle length, whereas DF work depended on both length and velocity during loading. These distal muscles appear to play a critical role in stability by rapidly sensing and responding to altered leg-ground interaction.
Following stroke, subjects retain the ability to adapt interlimb symmetry on the split-belt treadmill. Critical to advancing our understanding of locomotor adaptation and its usefulness in rehabilitation is discerning whether adaptive effects observed on a treadmill transfer to walking over ground. We examined whether aftereffects following split-belt treadmill adaptation transfer to overground walking in healthy persons and those poststroke.
Eleven poststroke and 11 age-matched and gender-matched healthy subjects walked over ground before and after walking on a split-belt treadmill. Adaptation and aftereffects in step length and double support time were calculated.
Both groups demonstrated partial transfer of the aftereffects observed on the treadmill (P<.001) to overground walking (P<.05), but the transfer was more robust in the subjects poststroke (P<.05). The subjects with baseline asymmetry after stroke improved in asymmetry of step length and double limb support (P=.06).
The partial transfer of aftereffects to overground walking suggests that some shared neural circuits that control locomotion for different environmental contexts are adapted during split-belt treadmill walking. The larger adaptation transfer from the treadmill to overground walking in the stroke survivors may be due to difficulty adjusting their walking pattern to changing environmental demands. Such difficulties with context switching have been considered detrimental to function poststroke. However, we propose that the persistence of improved symmetry when changing context to overground walking could be used to advantage in poststroke rehabilitation.
Gait adaptation is crucial for coping with varying terrain and biological needs. It is also important that any acquired adaptation is expressed only in the appropriate context. Here we review a recent series of experiments which demonstrate inappropriate expression of gait adaptation. We showed that a brief period of walking onto a platform previously experienced as moving results in a large forward sway despite full awareness of the changing context. The adaptation mechanisms involved in this paradigm are extremely fast, just 1-2 discrete exposures to the moving platform results in a motor after-effect. This after-effect still occurs even if subjects deliberately attempt to suppress it. However it disappears when the location or method of gait is altered, indicating that after-effect expression is context dependent. Conversely, making gait self-initiated increased sway during the after-effect. This after-effect demonstrates a profound dissociation between knowledge and action. The absence of generalisation suggests a simple form of motor learning. However, persistent expression of gait after-effects may be dependent on an intact cerebral cortex. The fact that the after-effect is greater during self-initiated gait, and is context dependent, would be consistent with the involvement of supraspinal areas.
We have previously shown an asymmetric generalization following a prism-induced visuomotor adaptation. Subjects who adapt to laterally deviating prism lenses during walking show a broad generalization to an arm pointing task, while subjects who adapt to prisms during arm pointing do not show generalization to walking. It is not known whether this broad generalization persists with other movements outside of walking or what specific features of the walking task, e.g. lower extremity involvement, allow it to be so broadly generalizable. In the current study, we tested healthy adult subjects performing one of three forms of prism adaptation and subsequently measured generalization. In Experiment 1 we tested whether a seated arm pointing prism adaptation would generalize to the leg. In Experiment 2 we tested whether a seated leg pointing prism adaptation would generalize to the arm. In Experiment 3 we tested whether standing influenced the extent of generalization from leg to arm. Results were surprising. We found a clear and consistent generalization from arm to leg, but much less so from leg to arm during either the seated or the standing task. These findings indicate that prism adaptations during arm movements are not limb-specific, as has been previously suggested. Further, the lack of generalization from leg to arm suggests that neither the adaptation of leg movements specifically, nor standing posture, nor the bilateral component of walking could be the salient feature allowing for its broad generalization across body parts.
Maintained 50 adult cats on Flaxedil after spinal transection at T-12 under ether anesthesia. Experimental Ss were classically conditioned by electrical stimulation of the exposed superficial peroneal nerve (CS), paired with cutaneous shock to the ankle of the same limb (UCS). The CR was the gross efferent volley recorded from the exposed deep peroneal nerve. Controls were divided into unpaired CS and UCS, CS-only, and UCS sensitization groups. Results show that the experimental conditions produced increases in amplitude of the gross efferent volley while unpaired CS and UCS, and CS-only control conditions produced no change or a decrease in amplitude. The UCS sensitization group showed that no sensitization was present at the intertrial intervals used in experimental conditions. (27 ref.)
Diverse roles in cellular functions have been ascribed to nitric oxide (NO), and its involvement in induction of long-term depression in cerebellar Purkinje cells has been demonstrated. Manipulations of NO concentration or its synthesis in cerebellar tissues therefore provide a means for investigating roles of NO in cerebellar functions at both cellular and behavioral levels. We tested adaptive control of locomotion to perturbation in cats, and found that this form of motor learning was abolished by application of either an inhibitor of NO synthase or a scavenger of NO to the cerebellar cortical locomotion area. This finding supports the view that NO in the cerebellum plays a key role in motor learning.
Previous studies have shown that stimulation of group 'I' afferents from ankle extensor muscles can prolong the cycle period in decerebrate walking cats and that the magnitude of these effects can be altered after chronic axotomy of the lateral-gastrocnemius/soleus (LGS) nerve. The effectiveness of LGS group I afferents in prolonging the cycle period decreases after axotomy, whereas the effectiveness of the uncut medial-gastrocnemius (MG) group I afferents is increased. The objectives of this investigation were to establish the time course of these changes in effectiveness and to determine whether these changes persist after transection of the spinal cord. The effects of stimulating the LGS and/or MG group I afferents on the cycle period were examined in 22 walking decerebrate animals in which one LGS nerve had been cut for 2 to 31 days. The effectiveness of LGS group I afferents declined progressively in the postaxotomy period, beginning with significant decreases at 3 days and ending close to zero effectiveness at 31 days. Large increases in the effectiveness of MG group I afferents occurred 5 days after axotomy, but there was no progressive change from 5 to 31 days. To test whether these changes in effectiveness were localized to sites within the spinal cord, the cord was transected in some decerebrate animals and stepping induced by the administration of L-DOPA L-3-4 dihydroxyphenylalanine (L-DOPA) and Nialamide. The effects of stimulating the MG and/or the LGS group I afferents on the cycle period were reexamined. In all four animals tested, stimulating the axotomized LGS group I afferents had a reduced effectiveness during locomotor activity in both the decerebrate and spinal states, whereas the increased effectiveness of the MG group I afferents was retained after transection of the spinal cord in two of five animals. Different mechanisms may be responsible for the changes in strength of the LGS and MG group I afferent pathways that project onto the rhythm generating sites in the spinal cord. This possibility follows from our observations of a linear relationship between the time after axotomy and decreased effectiveness of LGS group I afferents but no significant relationship between time postaxotomy and increased effectiveness of MG group I afferents; no significant relationship between the decreased effectiveness of LGS group I afferents and the increased effectiveness of MG group I afferents; and, after spinalization, consistent (4/4 cases) preservation of decreased LGS effectiveness but frequent (3/5 cases) loss of increased MG effectiveness.
This study examined the responses of cerebellar patients and a group of age- and sex-matched control subjects to repeated changes in treadmill speed in order to test whether cerebellar patients can adapt their gait to this type of perturbation and, if so, whether their responses are comparable to those of controls. While the subject walked on the treadmill, a perturbation consisting of a sudden slowing of the treadmill followed by a sudden increase back to the original speed was applied repeatedly at a specific time during the step cycle. Both the control subjects and cerebellar patients were able to compensate for the perturbations by minimizing their postural sway and changing step length. However, the nature of the compensatory changes in step length differed between these subject groups. Control subjects compensated for the perturbation by consistently using the same leg to initiate the response to the perturbation and by adapting a pattern of stepping such that the EMG characterizing the response occurred in a manner that was entrained to the timing of the normal locomotor cycle. In contrast, the patients, although undergoing modifications in step length, employed a much less consistent motor pattern from trial to trial than that of the normal subjects. An inconsistent pattern among their responses was apparent in both the analysis of stepping and in the EMG activity of the gastrocnemius and anterior tibial muscles. These results suggest that, although the cerebellar patients can adapt their behavior in response to locomotor perturbations, they do not establish a motor pattern comparable to that employed by normal subjects.
After lateral gastrocnemius-soleus (LGS) nerve section in intact cats, a rapid locomotor compensation involving synergistic muscles occurs and is accompanied by spinal reflex changes. Only some of these changes are maintained after acute spinalization, indicating the involvement of descending pathways in functional recovery. Here, we address whether the development of these adaptive changes is dependent on descending pathways. The left LGS nerve was cut in three chronic spinal cats. Combined kinematics and electromyographic (EMG) recordings were obtained before and for 8 d after the neurectomy. An increased yield at the ankle was present early after neurectomy and, as in nonspinal cats, was gradually reduced within 8 d. Compensation involved transient changes in step cycle structure and a longer term increase in postcontact medial gastrocnemius (MG) EMG activity. Precontact MG EMG only increased in one of three cats. In a terminal experiment, the influence of group I afferents from MG and LGS on stance duration was measured in two cats. LGS effectiveness at increasing stance duration was largely decreased in both cats. MG effectiveness was only slightly changed: increased in one cat and decreased in another. In cat 3, the plantaris nerve was cut after LGS recovery. The recovery time courses from both neurectomies were similar (p > 0.8), suggesting that this spinal compensation is likely a generalizable adaptive strategy. From a functional perspective, the spinal cord therefore must be considered capable of adaptive locomotor plasticity after motor nerve lesions. This finding is of prime importance to the understanding of functional plasticity after spinal injury.
Activity-dependent plasticity occurs in the spinal cord throughout life. Driven by input from the periphery and the brain, this plasticity plays an important role in the acquisition and maintenance of motor skills and in the effects of spinal cord injury and other central nervous system disorders. The responses of the isolated spinal cord to sensory input display sensitization, long-term potentiation, and related phenomena that contribute to chronic pain syndromes; they can also be modified by both classical and operant conditioning protocols. In animals with transected spinal cords and in humans with spinal cord injuries, treadmill training gradually modifies the spinal cord so as to improve performance. These adaptations by the isolated spinal cord are specific to the training regimen and underlie new approaches to restoring function after spinal cord injury. Descending inputs from the brain that occur during normal development, as a result of supraspinal trauma, and during skill acquisition change the spinal cord. The early development of adult spinal cord reflex patterns is driven by descending activity; disorders that disrupt descending activity later in life gradually change spinal cord reflexes. Athletic training, such as that undertaken by ballet dancers, is associated with gradual alterations in spinal reflexes that appear to contribute to skill acquisition. Operant conditioning protocols in animals and humans can produce comparable reflex changes and are associated with functional and structural plasticity in the spinal cord, including changes in motoneuron firing threshold and axonal conduction velocity, and in synaptic terminals on motoneurons. The corticospinal tract has a key role in producing this plasticity. Behavioral changes produced by practice or injury reflect the combination of plasticity at multiple spinal cord and supraspinal sites. Plasticity at multiple sites is both necessary-to insure continued performance of previously acquired behaviors-and inevitable-due to the ubiquity of the capacity for activity-dependent plasticity in the central nervous system. Appropriate induction and guidance of activity-dependent plasticity in the spinal cord is an essential component of new therapeutic approaches aimed at maximizing function after spinal cord injury or restoring function to a newly regenerated spinal cord. Because plasticity in the spinal cord contributes to skill acquisition and because the spinal cord is relatively simple and accessible, this plasticity is a logical and practical starting point for studying the acquisition and maintenance of skilled behaviors.
After sustained stepping in-place on a rotating disc, healthy subjects will inadvertently turn in circles when asked to step in-place on a stationary surface with eyes closed. We asked whether the cerebellum is important for this adaptive phenomenon, called podokinetic after-rotation (PKAR). Subjects with cerebellar degeneration and age-matched control subjects performed 15 min of stepping in-place with eyes open on a rotating disc, then 30 min of attempting to step in-place with eyes closed on a stationary surface. Rotational velocity of PKAR was measured during this 30-min period. All control subjects demonstrated PKAR; average initial rotational velocity for control subjects was 16.4+/-3.5 degrees /s. Five of the eight cerebellar subjects demonstrated impaired PK adaptation, defined as PKAR with an initial velocity more than two standard deviations below the control mean initial velocity. Average initial rotational velocity for cerebellar subjects was 7.8+/-0.2 degrees /s. Impaired PK adaptation was not associated with impaired time constants of decay and was not correlated with variability of PKAR velocity. Our results suggest that the cerebellum is important for regulation of the amplitude of PK adaptation and that reduced PKAR amplitude is not likely the result of dyscoordination or variability of movement in the subjects tested.
Load-related afferent information modifies the magnitude and timing of hindlimb muscle activity during stepping in decerebrate animals and spinal cord-injured humans and animals, suggesting that the spinal cord mediates load-related locomotor responses. In this study, we found that stepping on a treadmill by adult rats that received complete, midthoracic spinal cord transections as neonates could be altered by loading the hindlimbs using a pair of small robotic arms. The robotic arms applied a downward force to the lower shanks of the hindlimbs during the stance phase and measured the position of the lower shank during stepping. No external force was applied during the swing phase of the step. When applied bilaterally, this stance force field perturbed the hindlimb trajectories so that the ankle position was shifted downward during stance. In response to this perturbation, both the stance and step cycle durations decreased. During swing, the hindlimb initially accelerated toward the normal, unperturbed swing trajectory and then tracked the normal trajectory. Bilateral loading increased the magnitude of the medial gastrocnemius electromyographic (EMG) burst during stance and increased the amplitude of the semitendinosus and rectus femoris EMG bursts. When the force field was applied unilaterally, stance duration decreased in the loaded hindlimb, while swing duration was decreased in the contralateral hindlimb, thereby preserving interlimb coordination. These results demonstrate the feasibility of using robotic devices to mechanically modulate afferent input to the injured spinal cord during weight-supported locomotion. In addition, these results indicate that the lumbosacral spinal cord responds to load-related input applied to the lower shank during stance by modifying step timing and muscle activation patterns, while preserving normal swing kinematics and interlimb coordination.
Spatial-temporal gaze behaviour patterns were analysed as normal participants wearing a mobile eye tracker were required to step on 17 footprints, regularly or irregularly spaced over a 10-m distance, placed in their travel path. We examined the characteristics of two types of gaze fixation with respect to the participants' stepping patterns: footprint fixation; and travel fixation when the gaze is stable and travelling at the speed of whole body. The results showed that travel gaze fixation is a dominant gaze behaviour occupying over 50% of the travel time. It is hypothesised that this gaze behaviour would facilitate acquisition of environmental and self-motion information from the optic flow that is generated during locomotion: this in turn would guide movements of the lower limbs to the appropriate landing targets. When participants did fixate on the landing target they did so on average two steps ahead, about 800-1000 ms before the limb is placed on the target area. This would allow them sufficient time to successfully modify their gait patterns. None of the gaze behaviours was influenced by the placement (regularly versus irregularly spaced) of the footprints or repeated exposures to the travel path. Rather visual information acquired during each trial was used "de novo" to modulate gait patterns. This study provides a clear temporal link between gaze and stepping pattern and adds to our understanding of how vision is used to regulate locomotion.
We investigated the physiological basis of the 'broken escalator phenomenon', namely the sensation that when walking onto an escalator which is stationary one experiences an odd sensation of imbalance, despite full awareness that the escalator is not going to move. The experimental moving surface was provided by a linear motor-powered sled, moving at 1.2 m/s. Sled velocity, trunk position, trunk angular velocity, EMG of the ankle flexors-extensors and foot-contact signals were recorded in 14 normal subjects. The experiments involved, initially, walking onto the stationary sled (condition Before). Then, subjects walked 20 times onto the moving sled (condition Moving), and it was noted that they increased their walking velocity from a baseline of 0.60 m/s to 0.90 m/s. After the moving trials, subjects were unequivocally warned that the platform would no longer move and asked to walk onto the stationary sled again (condition After). It was found that, despite this warning, subjects walked onto the stationary platform inappropriately fast (0.71 m/s), experienced a large overshoot of the trunk and displayed increased leg electromyographic (EMG) activity. Subjects were surprised by their own behaviour and subjectively reported that the 'broken escalator phenomenon', as experienced in urban life, felt similar to the experiment. By the second trial, most movement parameters had returned to baseline values. The findings represent a motor aftereffect of walking onto a moving platform that occurs despite full knowledge of the changing context. As such, it demonstrates dissociation between the declarative and procedural systems in the CNS. Since gait velocity was raised before foot-sled contact, the findings are at least partly explained by open-loop, predictive behaviour. A cautious strategy of limb stiffness was not responsible for the aftereffect, as revealed by no increase in muscle cocontraction. The observed aftereffect is unlike others previously reported in the literature, which occur only after prolonged continuous exposure to a sensory mismatch, large numbers of learning trials or unpredictable catch trials. The relative ease with which the aftereffect was induced suggests that locomotor adaptation may be more impervious to cognitive control than other types of motor learning.
We have recently described a postural after-effect of walking onto a stationary platform previously experienced as moving, which occurs despite full knowledge that the platform will no longer move. This experiment involves an initial baseline period when the platform is kept stationary (BEFORE condition), followed by a brief adaptation period when subjects learn to walk onto the platform moving at 1.2 m/s (MOVING condition). Subjects are clearly warned that the platform will no longer move and asked to walk onto it again (AFTER condition). Despite the warning, they walk toward the platform with a velocity greater than that observed during the BEFORE condition, and a large forward sway of the trunk is observed once they have landed on the platform. This aftereffect, which disappears within three trials, represents dissociation of knowledge and action. In the current set of experiments, to gain further insight into this phenomenon, we have manipulated three variables, the context, location, and method of the walking task, between the MOVING and AFTER conditions, to determine how far the adaptation will generalize. It was found that when the gait initiation cue was changed from beeps to a flashing light, or vice versa, there was no difference in the magnitude of the aftereffect, either in terms of walking velocity or forward sway of the trunk. Changing the leg with which gait was initiated, however, reduced sway magnitude by approximately 50%. When subjects changed from forward walking to backward walking, the aftereffect was abolished. Similarly, walking in a location other than the mobile platform did not produce any aftereffect. However, in these latter two experiments, the aftereffect reappeared when subjects reverted to the walking pattern used during the MOVING condition. Hence, these results show that a change in abstract context had no influence, whereas any deviation from the way and location in which the moving platform task was originally performed profoundly reduced the size of the aftereffect. Although the moving platform aftereffect is an example of inappropriate generalization by the motor system across time, these results show that this generalization is highly limited to the method and location in which the original adaptation took place.
The ability to formulate explicit mathematical models of motor systems has played a central role in recent progress in motor control research. As a result of these modeling efforts and in particular the incorporation of concepts drawn from control systems theory, ideas about motor control have changed substantially. There is growing emphasis on motor learning and particularly on predictive or anticipatory aspects of control that are related to the neural representation of dynamics. Two ideas have become increasingly prominent in mathematical modeling of motor function--forward internal models and inverse dynamics. The notion of forward internal models which has drawn from work in adaptive control arises from the recognition that the nervous system takes account of dynamics in motion planning. Inverse dynamics, a complementary way of adjusting control signals to deal with dynamics, has proved a simple means to establish the joint torques necessary to produce desired movements. In this paper, we review the force control formulation in which inverse dynamics and forward internal models play a central role. We present evidence in its favor and describe its limitations. We note that inverse dynamics and forward models are potential solutions to general problems in motor control--how the nervous system establishes a mapping between desired movements and associated control signals, and how control signals are adjusted in the context of motor learning, dynamics and loads. However, we find little empirical evidence that specifically supports the inverse dynamics or forward internal model proposals per se. We further conclude that the central idea of the force control hypothesis--that control levels operate through the central specification of forces--is flawed. This is specifically evident in the context of attempts to incorporate physiologically realistic muscle and reflex mechanisms into the force control model. In particular, the formulation offers no means to shift between postures without triggering resistance due to postural stabilizing mechanisms.
Motor function is severely disrupted following spinal cord injury (SCI). The spinal circuitry, however, exhibits a great degree of automaticity and plasticity after an injury. Automaticity implies that the spinal circuits have some capacity to perform complex motor tasks following the disruption of supraspinal input, and evidence for plasticity suggests that biochemical changes at the cellular level in the spinal cord can be induced in an activity-dependent manner that correlates with sensorimotor recovery. These characteristics should be strongly considered as advantageous in developing therapeutic strategies to assist in the recovery of locomotor function following SCI. Rehabilitative efforts combining locomotor training pharmacological means and/or spinal cord electrical stimulation paradigms will most likely result in more effective methods of recovery than using only one intervention.
Previous investigations have demonstrated that feedback from ankle extensor group Ib afferents, arising from force-sensitive Golgi tendon organs, contributes to ankle extensor activity during the stance phase of walking in the cat. The objective of this investigation was to gain insight into the magnitude of this contribution by determining the loop gain of the positive force feedback pathway. Loop gain is the relative contribution of force feedback to total muscle activity and force. In decerebrate cats, the isolated medial gastrocnemius muscle (MG) was held at different lengths during sequences of rhythmic contractions associated with walking in the other three legs. We found that MG muscle activity and force increased at longer muscle lengths. A number of observations indicated that this length dependence was not due to feedback from muscle spindles. In particular, activity in group Ia afferents was insensitive to changes in muscle length during the MG bursts, and electrical stimulation of group II afferents had no influence on the magnitude of burst activity in other ankle extensors. We concluded that the homonymous positive force feedback pathway was isolated from other afferent pathways, allowing the use of a simple model of the neuromuscular system to estimate the pathway loop gain. This gain ranged from 0.2 at short muscle lengths to 0.5 at longer muscle lengths, demonstrating that force feedback was of modest importance at short muscle lengths, accounting for 20% of total activity and force, and of substantial importance at long muscle lengths, accounting for 50%. This length dependence was due to the intrinsic force-length property of muscle. The gain of the pathway that converts muscle force to motoneuron depolarization was independent of length. We discuss the relevance of this conclusion to the generation of ankle extensor activity in intact walking cats. These findings emphasize the general importance of feedback in generating ankle extensor activity during walking in the cat.
Numerous investigations over the past 15 years have demonstrated that sensory feedback plays a critical role in establishing the timing and magnitude of muscle activity during walking. Here we review recent studies reporting that sensory feedback makes a substantial contribution to the activation of extensor motoneurons during the stance phase. Quantitative analysis of the effects of loading and unloading ankle extensor muscles during walking on a horizontal surface has shown that sensory feedback can increase the activity of ankle extensor muscles by up to 60%. There is currently some uncertainty about which sensory receptors are responsible for this enhancement of extensor activity, but likely candidates are the secondary spindle endings in the ankle extensors of humans and the Golgi tendon organs in the ankle extensors of humans and cats. Two important issues arise from the finding that sensory feedback from the leg regulates the magnitude of extensor activity. The first is the extent to which differences in the magnitude of activity in extensor muscles during different locomotor tasks can be directly attributed to changes in the magnitude of sensory signals, and the second is whether the enhancement of extensor activity is determined primarily by feedback from a specific group of receptors or from numerous groups of receptors distributed throughout the leg. Limitations of current experimental strategies prevent a straightforward empirical resolution of these issues. A potentially fruitful approach in the immediate future is to develop models of the known and hypothesized neuronal networks controlling motoneuronal activity, and use these simulations to control forward dynamic models of the musculo-skeletal system. These simulations would help understand how sensory signals are modified with a change in locomotor task and, in conjunction with physiological experiments, establish the extent to which these modifications can account for changes in the magnitude of motoneuronal activity.
To gain insight into the neural mechanisms controlling different forms of quadrupedal walking of normal cats, data on postural orientation, hindlimb kinematics, and motor patterns of selected hindlimb muscles were assessed for four grades of upslope walking, from 25 to 100% (45 degrees incline), and compared with similar data for level treadmill walking (0.6 m/s). Kinematic data for the hip, knee, ankle, and metatarsophalangeal joints were obtained from digitizing ciné film that was synchronized with electromyographic (EMG) records from 13 different hindlimb muscles. Cycle periods, the structure of the step cycle, and paw-contact sequences were similar at all grades and typical of lateral-sequence walking. Also, a few half-bound and transverse gallop steps were assessed from trials at the 100% grade; these steps had shorter cycle periods than the walking steps and less of the cycle (68 vs. 56%) was devoted to stance. Each cat assumed a crouched posture at the steeper grades of upslope walking and stride length decreased, whereas the overall position of the stride shifted caudally with respect to the hip joint. At the steeper grades, the range and duration of swing-related flexion increased at all joints, the stance-phase yield was absent at the knee and ankle joints, and the range of stance-phase extension at knee and ankle joints increased. Patterns of muscle activity for upslope and level walking were similar with some notable exceptions. At the steeper grades, the EMG activity of muscles with swing-related activity, such as the digit flexor muscle, the flexor digitorum longus (FDL), and the knee flexor muscle, the semitendinosus (ST), was prolonged and continued well into midswing. The EMG activity of stance-related muscles also increased in amplitude with grade, and three muscles not active during the stance phase of level walking had stance activity that increased in amplitude and duration at the steepest grades; these muscles were the ST, FDL, and extensor digitorum brevis. Overall the changes in posture, hindlimb kinematics, and the activity patterns of hindlimb muscles during upslope walking reflected the need to continually move the body mass forward and upward during stance and to ensure that the paw cleared the inclined slope during swing. The implications of these changes for the neural control of walking and expected changes in hindlimb kinetics for slope walking are discussed.
When a suspended headless large insect (cockroach or locust) is arranged so that the leg receives a regularly repeated electric shock for all the time that the foot falls below a particular position, there is a progressive change in the animal's behaviour over a period of about half an hour. The animal at first receives many shocks but progressively raises its leg for longer and longer intervals, with the result that fewer shocks are received. A second animal is arranged in series with the first, and receives the same shocks but in this animal they are not related to a particular position of the foot. Therefore, the second animal cannot associate the shocks with the position of the foot at the moment when they are received, in the way that the first has an opportunity to do. After an initial training period of 40 to 45 min the two animals are disconnected and reconnected in parallel to the stimulator so that each now separately receives a shock when its leg falls below a critical position. When retested in this way the first animals of each pair receive less shocks than do the second animals, especially at the start of the retest before the second animal of the pair has had an opportunity to make an association in the course of the retest. Similar results are obtained when the animals are trained on one leg and retested on another leg on a different segment. The conclusion is that in the absence of a brain the ventral ganglia are able to associate a position of the leg with a repeated punishment by electric shock.
A number of internal model concepts are now widespread in neuroscience and cognitive science. These concepts are supported by behavioral, neurophysiological, and imaging data; furthermore, these models have had their structures and functions revealed by such data. In particular, a specific theory on inverse dynamics model learning is directly supported by unit recordings from cerebellar Purkinje cells. Multiple paired forward inverse models describing how diverse objects and environments can be controlled and learned separately have recently been proposed. The 'minimum variance model' is another major recent advance in the computational theory of motor control. This model integrates two furiously disputed approaches on trajectory planning, strongly suggesting that both kinematic and dynamic internal models are utilized in movement planning and control.
To gain further insight into the neural mechanisms for different forms of quadrupedal walking, data on postural orientation, hindlimb kinematics, and motor patterns were assessed for four grades of downslope walking, from 25% (14 degrees slope) to 100% (45 degrees), and compared with data from level and downslope walking at five grades (5-25%) on the treadmill (0.6 m/s). Kinematic data were obtained by digitizing ciné film, and electromyograms (EMGs) synchronized with kinematic records were taken from 13 different hindlimb muscles. At grades from 25 to 75%, cycle periods were similar, but at the steepest grade the cycle was shorter because of a reduced stance phase. Paw-contact sequences at all grades were consistent with lateral-sequence walking, but pace walking often occurred at the steepest grades. The cats crouched at the steeper grades, and crouching was associated with changes in fore- and hindlimb orientation that were consistent with increasing braking forces and decreasing propulsive forces during stance. The average ranges of motion at the hindlimb joints, except at the hip, were often different at the two steepest slopes. During swing, the range of knee- and ankle-joint flexion decreased, and the range and duration of extension increased at the ankle joint to lower the paw downward for contact. During stance the range of flexion during yield increased at the ankle joint, and the range of extension decreased at the knee and metatarsophalangeal joints. Downslope walking was also associated with EMG changes for several muscles. The hip extensors were not active during stance; instead, hip flexors were active, presumably to slow the rate of hip extension. Although ankle extensors were active during stance, their burst durations were truncated and centered around paw contact. Ankle flexors were active after midstance at the steeper slopes before the need to initiate swing, whereas flexor and extensor digit muscles were coactive throughout stance. Overall the changes in posture, hindlimb kinematics, and activity patterns of hindlimb muscles during stance reflected a need to counteract external forces that would accelerate angular displacements at some joints. Implications of these changes are discussed by using current models for the neural control of walking.
1. Tactile stimuli to the paw consisting of a stick making contact or an air puff aimed at the dorsum were used to study the phasic influence of locomotor activity on the reflex pattern elicited in extensor and flexor muscles and on the induced compensatory movements in intact cats. The resulting movements and reflex pattern are called "stumbling corrective reactions." 2. The basic reflex pattern and movements of the stumbling corrective reaction are: a) if the stimulus occurs during the swing phase, a short-latency activation of the flexor muscles, which induces an additional flexion of the limb lifting the paw over the obstacle; b) if the stimulus occurs during the support phase, an inhibition followed by an excitation of the extensor muscles, which neither increase nor decrease the extension. However, the stimulus evokes an increased flexor activity in the succeeding swing phase, which induces a brisker flexion. 3. Tactile stimuli to the proximal part of the limb or to the belly in front of the knee evoked the same type of phase-dependent compensatory reactions. Such reactions would presumably be beneficial for the animal to avoid high obstacles that impede movement. 4. A nonnoxious electrical stimulus (typically 2 mA; 1 ms) applied to the dorsum of the paw was used to study systematically the reflex pattern of the stumbling corrective reaction. Two pathways were defined to the knee flexor (semitendinosus). One early burst was evoked at about 10 ms and one later at about 25 ms after the stimulus. Short inhibitory pathways and longer excitatory pathways (20-50 ms) projected to the extensor nuclei. A short-latency (10 ms) excitatory pathway to the ankle extensor (lateral gastrocnemius) was also activated. 5. A painful electrical stimulus applied to the dorsum of the paw evoked large flexor responses during the whole step cycle. During the support phase the locomotion was disrupted as the supporting limb was withdrawn. 6. The results demonstrate that intact cats are able to compensate rapidly for unpredicted perturbations and that the reflex pattern and the induced corrective movements are adapted to the locomotor activity so that functionally meaningful movements are evoked in each phase of the step cycle. 7. The evoked reflexes and their modulation are consistent with those previously found in chronic spinal cats during walking and in paralyzed spinal cats performing "fictive locomotion." It is suggested that the same spinal pathways are used, and that they are controlled by the spinal "locomotor generator."
1. The ability of somaesthetic sensory inputs to produce structural changes in the connectivities of the central nervous structures involved in motor activity was tested with an alpha type of classical conditioning in chronically prepared adult cats. Repetitive sensory stimulation was applied at constant intervals after the activation of the motor circuits originating in the neurons or efferent axons of the cerebellar nuclei. A conditional stimulation (CS) applied to interpositus neurons was consistently paired with an unconditional stimulation (UCS) applied to the dorsal skin of the forelimb extremity to induce associative sensorimotor conditioning. The sites at which the conditional and unconditional stimuli were applied set up a simplified sensorimotor circuit including pathways transmitting both these stimuli and others mediating the expression of the conditioned responses. 2. To test the changes resulting from the conditioning, electrodes were implanted into the various relay structures on the cerebellar efferent pathways (ventrolateral nucleus motor cortex). The forelimb motor responses elicited by stimulating these relay structures were recorded with a potentiometer placed at the elbow joint. The angular displacement (amplitude) and latency of the responses and the percentage response rates were systematically quantified throughout the conditioning procedure and at test sessions carried out after the daily conditioning routines. 3. It was observed that daily repetition of paired CS-UCS led to an increase in the response rates and amplitudes of the forelimb flexions, which already began to occur very slightly on the first 4 or 5 days in response to the alpha conditioning, whereas the CS when applied alone failed to produce any changes in this initial response. Likewise, after the acquisition phase, repeated presentation of either the CS alone or the CS preceded by the UCS led to the extinction of the conditioned response, thus indicating that the observed changes were of an associative nature and that they depended on interactions between the motor and sensory inputs occurring somewhere in the CNS. In fact, the effects of conditioning were not generalized, but involved only a circumscribed circuit originating in the cerebellar neurons stimulated by the CS, which were activated concomitantly with the sensory pathways. 4. The conditioned response amplitudes were enhanced by 2.5-3 times their initial value. This enhancement persisted at the end of acquisition or after several days of consolidation, even when the paired CS-UCS sessions were interrupted for a period of 15 days to 2 mo.(ABSTRACT TRUNCATED AT 400 WORDS)
Experiments were performed in ambulating decerebrate ferrets to examine the activity of up to 6 simultaneously recorded Purkinje cells oriented sagittally during unperturbed and perturbed locomotion using a new analytical technique, the real-time postsynaptic response (RTPR), which permits a trial-by-trial assessment of the action of the recorded neurons on a simulated cerebellar nuclear cell. The data illustrate that the responsiveness of the Purkinje cells located in a specific region of lobules V and VI is most dramatically modulated by the perturbations of the locomotor cycle and that this responsiveness in the perturbed trials is related to the degree of synchrony of the activated climbing fiber inputs to the cells of the set. The data were interpreted as supporting the gain change hypothesis of climbing fiber function.
These experiments address the hypothesis that the trajectory of a forelimb in decerebrate ambulating ferrets can be conditioned to avoid an obstacle encountered during the locomotor cycle. The perturbation was produced by interjecting a bar into the trajectory of the forelimb during swing phase. Over 5-15 steps the flexion of the elbow progressively increased until the forelimb was elevated over the bar. Avoiding the bar often required that the maximum height of the paw during swing phase was doubled. When the bar was no longer thrust into the trajectory of the forelimb, the conditioned behavior persisted for several step cycles. The results indicate that decerebrate ferrets are capable of acquiring a conditioned limb movement that is not a typical conditioned reflex but rather an accentuation of a component of the step cycle performed to avoid an interruption of swing phase.
These experiments were performed to examine the relationship between the simple and complex spike responses of 3-5 simultaneously recorded Purkinje cells during the acquisition, performance and extinction of a conditioned forelimb movement in decerebrate, unanesthetized ferrets. The data demonstrate parallel, correlated changes in simple and complex spike responses throughout the experimental period. Since the evaluated Purkinje cells were examined in the cerebellar cortical region that contains neurons highly modulated by the intermittent application of the conditioning stimulus, these findings argue against an induction of a long-lasting modification in simple spike responses by the climbing fiber input as the basis for this type of motor learning.
The anatomy, architecture, and innervation patterns of the hamstring muscles, biceps femoris, and semitendinosus were examined in adult cats using microdissection and glycogen-depletion techniques. The biceps femoris muscle consists of two heads. The anterior head, which attaches mainly to the femur, is divided into two parts by the extramuscular branches of its nerve. The posterior head is innervated by a single nerve. Semitendinosus is composed of two heads, one proximal and one distal to a tendinosus inscription, each of which is separately innervated. The extramuscular branches of the nerves to these hamstring muscles thus partition them into innervation subvolumes termed parts. The available evidence suggests that each of the parts of these muscles so innervated is not equivalent to the collections of single motor units that have been described for ankle extensors as neuromuscular compartments. It is quite likely that each of the parts of the hamstring muscles may contain more than one neuromuscular compartment. Using chronically implanted EMG electrodes, the activation patterns of different parts of the hamstring muscles were analyzed during locomotion. The anterior and middle parts of biceps femoris are active during the early stance phase, probably producing hip extensor torque. The posterior part of biceps femoris and semi-tendinosus act most consistently as flexors, during the early swing phase, but also may function in synergy with hip, knee, and ankle joint extensors near the time of foot placement. Greater variability is found in the activity patterns of posterior biceps femoris and semitendinosus with respect to the kinematics of the step cycle than is observed for anterior and middle biceps femoris. It is suggested that this variation may reflect a larger role of sensory feedback in shaping the timing of activity in posterior biceps femoris and semitendinosus than in "nonarticular" muscles.
Cats were spinalized (T13) as adults and were trained to walk with the hindlimbs on a treadmill. After 3 weeks to 3 months and up to 1 year depending on the animal, all were capable of walking on the plantar surface of the feet and support the weight of the hindquarters. Interactive training appeared to accelerate the recovery of locomotion and maintain smooth locomotor movements. Despite the obvious loss of voluntary control and equilibrium which the experimenter partially compensated for by maintaining the thorax and/or the tail, the cats could walk with a regular rhythm and a well-coordinated hindlimb alternation at speeds of 0.1-1.2 m/s. Cycle duration as well as stance and swing duration resembled those of normal cats at comparable speeds. The range of angular motion was also similar to that observed in intact cats as was the coupling between different joints. The EMG activity of the hindlimb and lumbar axial muscles also retained the characteristics observed in the intact animal. Some deficits such as a dragging of the foot in early swing and diminution of the angular excursion in the knee were seen at later stages. Thus, the adult spinal cat preparation is considered as a useful model to study the influence of different types of training and of different drugs or other treatments in the process of locomotor recovery after injury to the spinal cord.
If an obstacle impedes the forward swing of a cat's foot, the animal responds by rapidly lifting the foot over the obstacle. In freely moving cats, the electrical activity of hindlimb flexors and extensors was recorded during such reactions elicited both mechanically and electrically. The sequencing of muscle activity was more complex and longer in duration in the mechanically elicited reactions. Anaesthesia of the foot dorsum abolished responses in ankle extensors and knee flexors, and converted the responses of ankle flexors to simple stretch reflexes. Although our findings closely resemble those reported for chronic spinal kittens, there are interesting points of difference, which should be taken into account if the notion of a purely spinal mediation of the placing reaction during stepping is to be accepted.
Classically conditioned facilitation of the flexor withdrawal reflex of spinal cat occurs in knee and ankle flexor muscles but not in a flexor muscle of the toes. Furthermore, the spinal circuitry activated by a component of the conditioned stimulus (A alpha cutaneous fibers) is not by itself involved in the reflex conditioning. The results suggest that increases in both cutaneous afferent output and motoneuron excitability may be eliminated as mechanisms contributing to conditioning and point to certain interneuronal pools as the locus of learning in this preparation.
Eight human subjects were exposed to 2 h of walking on the perimeter of a horizontally rotating disc with the body remaining still in space. After adaptation to this experience subjects were blindfolded and asked to walk straight ahead on firm ground. When doing so all subjects generated curved walking trajectories of radii ranging from 65 to 200 inches and angular velocities from 7 to 20 deg/s. Subsequent trials over the next half hour revealed retained, but decreasing, trajectory curvature. Angular velocities associated with these trajectories were well above vestibular sensory threshold, yet all subjects consistently perceived themselves as walking straight ahead. The blindfolded subjects were also asked to propel themselves in a straight line in a wheel chair. Post-adaptation wheel chair trajectories showed no change from those before adaptation. Hence we infer that it was the relation between somatosensory/motor elements of gait and the perception of trunk rotation that had been remodelled during walking on the turning disc. This novel form of adaptive plasticity presumably serves to maintain optimal values of central neural parameters that control the trajectory of locomotion. The findings may have significant implications for the diagnosis and rehabilitation of locomotor and vestibular disorders.
1. To determine whether the motor cortex is involved in the modification of the hindlimb trajectory during voluntary adjustments of the locomotor cycle, we recorded the discharge patterns of 72 identified pyramidal tract neurons (PTNs) within the hindlimb region of pericruciate area 4 during a task in which cats stepped over obstacles attached to a moving treadmill belt. Data were also recorded from representative flexor and extensor muscles of the fore- and hindlimbs contralateral to the recording site. 2. To step over the obstacles, the cats increased flexion sequentially at the knee, ankle, and then the hip to bring the leg above and over the obstacle. This flexion movement was followed by a strong extension of the whole limb that repositioned the foot on the treadmill belt. These changes in limb trajectory were associated with large changes in the level of the activity of many flexor and extensor muscles of the hindlimb, and especially of the knee flexor, semitendinosus. On the basis of the time of onset of the knee and ankle extensor muscles in those steps when the limb was the first to be brought over the obstacle, the swing phase of the modified step cycle was subdivided into two parts, Phase I and Phase II, which correspond respectively to the flexion of the limb (F) and the initial extension (E1). 3. The temporal sequence of the movement was the same whether the hindlimb was the first (lead) or second (trail) to step over the obstacle, although the relative time between flexion at the three joints was changed in the two conditions. 4. Seventy-two PTNs were recorded from the posterior bank of the cruciate sulcus during the voluntary gait modifications. Sixty-three (63/72) of these PTNs had receptive fields that were confined to the contralateral hindlimb, or were recorded from penetrations in which such cells were found. Nine (9/72) PTNs had receptive fields on both the contralateral fore- and hindlimbs. Microstimulation applied through the recording electrode evoked, in all cases, brief twitch responses only in contralateral hindlimb musculature. 5. Forty-two (42/63) of those PTNs with receptive fields confined to the hindlimb showed a significant increase in their discharge frequency when the limb contralateral to the recording site was the first to step over the obstacle (lead limb). Twenty-nine PTNs (29/63) discharged maximally during the swing phase (18 in Phase I and 11 in Phase II), including two PTNS that also increased their discharge frequency during stance.(ABSTRACT TRUNCATED AT 400 WORDS)
Recent research in the field of spinal pattern generation has concentrated on three main areas: the effects of various transmitters on spinal rhythmic patterns in reduced preparations (neonatal rats, chick embryos, tadpole embryos, lampreys); the changes in membrane properties of different elements of the generating circuits; and the interactions between central generating mechanisms and afferent inputs. The important message is that new properties of neural membranes, as well as new reflex responses, have been identified that could not have been predicted in the absence of such rhythmic activity.
1. Four cats were trained to walk backward (BWD) and forward (FWD) on a motorized treadmill. Mechanical (taps) or electrical (pulses) stimuli were applied to the dorsal or ventral aspect of the hind paw during swing or stance. Hindlimb kinematic data, obtained by digitizing 16-mm high-speed film, were synchronized with computer-analyzed electromyograms (EMG) recorded from anterior biceps femoris (ABF), vastus lateralis (VL), lateral gastrocnemius (LG), tibialis anterior (TA), and semitendinosus (ST). Responses to taps and pulses, as well as the modulation in cutaneous reflex sensitivity to pulses, were described for both walking directions and stimulus locations. 2. After dorsal taps that obstructed FWD swing, the hindlimb initially drew back away from the obstacle with knee flexion and ST activation, ankle extension with TA suppression and LG activation, and hip extension with ABF facilitation. Next, the limb was raised over the obstacle with resumed TA activity and enhanced knee and ankle flexion, and then compensatory knee and ankle extension positioned the limb for the ensuing stance phase. 3. For ventral taps that obstructed BWD swing, the initial response also tended to draw the limb away from the obstacle with hip and ankle flexion and TA facilitation and reduced knee flexion with weak VL facilitation and suppression of ST activity. Next, ST activity resumed as knee and ankle flexion raised the limb over the obstacle, and then compensatory extension completed the swing phase for BWD walking. Thus the initial kinematic and EMG responses to obstacles were opposite for BWD versus FWD swing, and these responses were consistent with active avoidance of the obstacles. Responses during BWD walking were subtle, however, compared with those for FWD. 4. After nonobstructing taps (ventral FWD, dorsal BWD), ST and TA activation and knee and ankle flexion were coincident, demonstrating that the aforementioned differences in responses to obstructing obstacles were not simply location dependent. Regardless of the direction of walking or the location of stimulation, taps applied during stance had little immediate kinematic effect, but the subsequent swing phase was usually exaggerated, as if the response was programmed to avoid any lingering obstacle. 5. Electrical pulses did not elicit the full-blown responses typically evoked by taps. The sequencing in activation of ST and TA characteristic after laps was absent after pulses, and there were rarely dramatic kinematic responses to pulses like those easily elicited by taps. There were, in fact, few differences in responses to electrical stimulation for BWD versus FWD walking.(ABSTRACT TRUNCATED AT 400 WORDS)
We investigated how human subjects adapt to forces perturbing the motion of their ams. We found that this kind of learning is based on the capacity of the central nervous system (CNS) to predict and therefore to cancel externally applied perturbing forces. Our experimental results indicate: (i) that the ability of the CNS to compensate for the perturbing forces is restricted to those spatial locations where the perturbations have been experienced by the moving arm. The subjects also are able to compensate for forces experienced at neighboring workspace locations. However, adaptation decays smoothly and quickly with distance from the locations where disturbances had been sensed by the moving limb. (ii) Our experiments also how that the CNS builds an internal model of the external perturbing forces in intrinsic (muscles and / or joints) coordinates.
One important aspect of locomotor control is the ability of an animal to make anticipatory gait modifications to avoid obstacles, by stepping either around them or over them. This paper reviews some of the evidence that suggests that the motor cortex is one of the principal structures involved in the control of such anticipatory gait modifications in cats, in particular when they are triggered by a visual signal. Evidence for this statement is provided both from experiments in which the motor cortex has been lesioned or inactivated and from studies in which the activity of motor cortical neurones has been recorded during locomotor tasks in which visual information is required to ensure the correct positioning of the paw or an appropriate modification of the limb trajectory. Inactivation of small regions of the motor cortex with the GABA agonist muscimol results in changes in the limb trajectory so that cats hit an obstacle instead of stepping over it as they do normally. A similar disruption of the hindlimb trajectory is seen following lesions of the spinal cord at T13 that interrupt the corticospinal tract. The results from cell recording studies are complementary in that they show that the activity of many identified pyramidal tract neurones increases when the cat is required to modify the forelimb or hindlimb trajectory to step over obstacles. We suggest that the major function of this increased discharge frequency is to regulate the amplitude, duration, and temporal pattern of muscle activity during the gait modification to ensure an appropriate modification of limb trajectory. We further suggest that different groups of pyramidal tract neurones are involved in regulating the activity of groups of synergistic muscles active at different times in the gait modification. For example, some groups of pyramidal tract neurones would be involved in ensuring the appropriate and sequential activation of the muscle groups involved in the initial flexion of the elbow, while others would be active prior to the repositioning of the paw on the support surface. We discuss the possibility that the motor cortical activity seen during locomotion is the sum result of a feedforward signal, which provides visuospatial information about the environment, and feedback activity, which signals, in part, the state of the interneuronal pattern generating networks in the spinal cord. The way in which the resulting descending command may interact with the basic locomotor rhythm to produce the gait modifications is discussed.
Split-belt locomotion (i.e., walking with unequal leg speeds) requires a rapid adaptation of biomechanical parameters and therefore of leg muscle electromyographic (EMG) activity. This adaptational process during the first strides of asymmetric gait as well as learning effects induced by repetition were studied in 11 healthy volunteers. Subjects were switched from slow (0.5 m/s) symmetric gait to split-belt locomotion with speeds of 0.5 m/s and 1.5 m/s, respectively. All subjects were observed to adapt in a similar way: (1) during the first trial, adaptation required about 12-15 strides. This was achieved by an increase in stride cycle duration, i.e., an increase in swing duration on the fast side and an increase in support duration on the slow side. (2) Adaptation of leg extensor and flexor EMG activity paralleled the changes of biomechanical parameters. During the first strides, muscle activity was enhanced with no increase in coactivity of antagonistic leg muscles. (3) A motor learning effect was seen when the same paradigm was repeated a few minutes later--interrupted by symmetric locomotion--as adaptation to the split-belt speeds was achieved within 1-3 strides. (4) This short-time learning effect did not occur in the "mirror" condition when the slow and fast sides were inverted. In this case adaptation again required 12-15 strides. A close link between central and proprioceptive mechanisms of interlimb coordination is suggested to underlie the adaptational processes during split-belt conditions. It can be assumed that, as in quadrupedal locomotion of the cat, human bipedal locomotion involves separate locomotor generators to provide the flexibility demanded. The present results suggest that side-specific proprioceptive information regarding the dynamics of the movement is necessary to adjust the centrally generated locomotor activity for both legs to the actual needs for controlled locomotion. Although the required pattern is quickly learned, this learning effect cannot be transferred to the contralateral side.
To study the potential plasticity of locomotor networks in the spinal cord, an important issue for locomotor rehabilitation after spinal injuries, we have investigated the locomotor performance of cats before and after a unilateral denervation of the ankle flexors tibialis anterior (TA) and extensor digitorum longus (EDL) both in cats with intact spinal cord and after spinalization. The effects of the inactivation of the ankle flexors were studied in three cats with intact spinal cord during periods of 4-7 wk. Cats adapted their locomotor performance very rapidly within a few days so that the locomotor behavior appeared to be unchanged practically. However, kinematic analyses of video records often revealed small but consistent increase in knee and/or hip flexion. These changes were accompanied by some increase in the amplitude of knee and hip flexor muscle activity. Cats maintained a regular and symmetrical walking pattern over the treadmill for several minutes. Two of these cats then were spinalized at T13 and studied for approximately 1 mo afterward. Whereas normally cats regain a regular and symmetrical locomotor pattern after spinalization, these cats had a disorganized and asymmetrical locomotor pattern with a predominance of knee flexion and absence of plantar foot contact of the denervated limb. Another cat first was spinalized and allowed to recuperate a regular symmetrical locomotor performance. Then it also was submitted to the same unilateral ankle flexor inactivation and studied for approximately 50 days. The cat maintained a well-organized symmetrical gait although there was almost no ankle flexion on the denervated side. There was no exaggerated knee hyperflexion and gait asymmetry as seen in the two previous cats spinalized only after they had adapted to the denervation of ankle flexors. It is concluded that, after muscle denervation, locomotor adaptation is achieved through changes occurring at different levels. Because cats spinalized after adaptation to the neurectomy had an asymmetrical locomotor pattern dominated by hyperflexion, it is suggested that the spinal circuitry has been modified during the adaptive process, presumably through the action of corrective supraspinal inputs. Indeed spinal cats do not normally display such abnormal hyperflexions, and neither did the one cat denervated after spinalization. On the other hand, because the modified locomotor pattern in the spinal state is not functional and contains only some aspects of the compensatory response seen before spinalization, it is suggested that the complete functional adaptation observed in intact cats after peripheral nerve lesions may depend on changes occurring at the spinal and the supraspinal levels.
The modification of the normal locomotor pattern of humans was investigated using a split-belt locomotion protocol (treadmill belt speeds of 4.5 km/h and 1.5 km/h for the right and left legs, respectively) and also by changing afferent input from the legs (30% reduction or increase in body weight by suspending subjects in a parachute harness or by wearing a lead-filled vest). After a control-speed training period (10 min) of symmetrical walking (3 km/h each leg) and a period (10 min) of split-belt walking, the adjustment back to the control speed resulted in a mean speed difference between the right leg and the left leg of 0.85 km/h. Adjustment of belt speed on either side was performed by the hands using a potentiometer. For comparison, also speed adjustment by the feet via feedback derived from changes in the treadmill drive current was studied. No significant difference was obtained when both modes of adjustment were compared. Body unloading or loading during the training period resulted in an improved adjustment of treadmill belt speed. This suggests that load receptor information plays a major role in the programming of a new walking pattern.
The present study characterizes a previously reported adaptive phenomenon in a somatosensory-motor system involved in directional control of locomotor trajectory through foot contact with the floor. We call this the "podokinetic" (PK) system. Podokinetic adaptation was induced in six subjects by stepping in-place over the axis of a horizontally rotating disc over a range of disc angular velocities (11.25-90 degrees/s) and durations (7.5-60 min). After adaptation, subjects were blindfolded and attempted to step in-place on the floor without turning. Instead they all rotated relative to space. The rate of the "podokinetic afterrotation" (PKAR) was linearly related to stimulus amplitude up to 45 degrees/s, and the ratio of initial PKAR velocity to that of the adaptive stimulus was approximately 1:3. PKAR exhibited exponential decay, which was composed of "short-" and "long-term" components with "discharging" time constants on the order of 6-12 min and 1-2 h, respectively. The effect of stimulus duration on PKAR revealed a "charging" time constant that approximated that of the short-term component. A significant suppression of PKAR occurred during the 1 st min of the postadaptive response, suggesting functional interaction between the PK and vestibular systems during the period of vestibular stimulation. During PKAR subjects perceived no self-rotation, indicating that perception as well as locomotor control of spatial orientation were remodeled by adaptation of the PK system.
Several "locomotor regions" of the mammalian brain stem can be stimulated, either electrically or chemically, to induce locomotion. Active cells labeled with c-fos within the mesencephalic locomotor region (MLR) have been found in the periaqueductal gray, the cuneiform nucleus, the pedunculopontine nucleus, and the locus coeruleus. Different subsets of these nuclei appear to be activated during locomotion produced in different behavioral contexts. The locomotor nuclei can be classified into areas associated with exploratory, appetitive, and defensive locomotion, in accordance with the proposal of Sinnamon (1993, Prog. Neurobiol. 41: 323-344). The interpretation of lesion studies designed to reveal areas of the brain essential for locomotion must be based on knowledge of the nuclei which become active in the specific locomotor task being tested. An argument is put forward in favor of the continued use of the term "mesencephalic locomotor region."
In this investigation we have estimated the afferent contribution to the generation of activity in the knee and ankle extensor muscles during walking in decerebrate cats by loading and unloading extensor muscles, and by unilateral deafferentation of a hind leg. The total contribution of afferent feedback to extensor burst generation was estimated by allowing one hind leg to step into a hole in the treadmill belt on which the animal was walking. In the absence of ground support the level of activity in knee and ankle extensor muscles was reduced to approximately 70% of normal. Activity in the ankle extensors could be restored during the "foot-in-hole" trials by selectively resisting extension at the ankle. Thus feedback from proprioceptors in the ankle extensor muscles probably makes a large contribution to burst generation in these muscles during weight-bearing steps. Similarly, feedback from proprioceptors in knee extensor appears to contribute substantially to the activation of knee extensor muscles because unloading and loading these muscles, by lifting and dropping the hindquarters, strongly reduced and increased, respectively, the level of activity in the knee extensors. This conclusion was supported by the finding that partial deafferentation of one hind leg by transection of the L4-L6 dorsal roots reduced the level of activity in the knee extensors by approximately 50%, but did not noticeably influence the activity in ankle extensor muscles. However, extending the deafferentation to include the L7-S2 dorsal roots decreased the ankle extensor activity. We conclude that afferent feedback contributes to more than one-half of the input to knee and ankle extensor motoneurons during the stance phase of walking in decerebrate cats. The continuous contribution of afferent feedback to the generation of extensor activity could function to automatically adjust the intensity of activity to meet external demands.
The cerebellar interposed nuclei are considered critical components of circuits controlling the classical conditioning of eyeblink responses in several mammalian species. The main purpose of the present experiments was to examine whether the interposed nuclei are also involved in the control of classically conditioned withdrawal responses in other skeletomuscular effector systems. To achieve this objective, a unique learning paradigm was developed to examine classically conditioned withdrawal responses in three effector systems (the eyelid, forelimb and hindlimb) in individual cats. Trained animals were injected with muscimol in the cerebellar interposed nuclei, and the effects on the three conditioned responses (CRs) were examined. Although the effects of muscimol were less dramatic than previously reported in the rabbit eyeblink preparation, the inactivation of the cerebellar nuclei affected the performance of CRs in all three effector systems. In additional experiments, animals were injected with muscimol at the sites affecting classically conditioned withdrawal responses to determine the effects of these injections on reaching and locomotion behaviors. These tests demonstrated that the same regions of the cerebellar interposed nuclei which control withdrawal reflexes are also involved in the control of limb flexion and precision placement of the paw during both locomotion and reaching tasks. The obtained data indicate that the interposed nuclei are involved in the control of ipsilateral action primitives and that inactivating the interposed nuclei affects several modes of action of these functional units.
A basic aspect of the neuronal control of quadrupedal locomotion of cat and of bipedal stance and gait of humans concerns the antigravity function of leg extensors. In humans proprioceptive reflexes involved in the maintenance of body equilibrium depend on the presence of contact forces opposing gravity. Extensor load receptors are thought to signal changes of the projection of body's centre of mass with respect to the feet. According to observations in the cat, this afferent input probably arises from Golgi tendon organs and represents a newly discovered function of these receptors in the regulation of stance and gait. From these experiments it can be concluded that during locomotion there is a closing of Ib inhibitory and an opening of Ib extensor facilitatory paths. In humans evidence for a significant contribution of load receptor contribution to the leg muscle activation came from immersion experiments. Compensatory leg muscle activation depends on the actual body weight. Also during gait the strength of leg extensor activation during the stance phase is load dependent. In patients with Parkinson's disease there is a reduced load sensitivity and decreased leg extensor activation, which might contribute to the movement disorder. Recent experiments in paraplegic patients show that the beneficial effects of a locomotor training critically depends on the initial degree of body unloading and reloading during the course of the training period.
Unifying principles of movement have emerged from the computational study of motor control. We review several of these principles and show how they apply to processes such as motor planning, control, estimation, prediction and learning. Our goal is to demonstrate how specific models emerging from the computational approach provide a theoretical framework for movement neuroscience.
Falls due to slips are prevalent in everyday life. The purpose of this study was to determine the reactive recovery responses used to maintain dynamic stability during an unexpected slip, establish the time course of response adaptation to repeated slip perturbations, and distinguish the proactive strategies for negotiating a slippery surface. Twelve young adults participated in the study in which a slip was generated following foot contact on a set of steel free-wheeling rollers. Surface electromyographic (EMG) data were collected from rectus femoris, biceps femoris, tibialis anterior, and the medial head of gastrocnemius on the perturbed limb. Whole body kinematics were recorded using an optical imaging system: from this the center of mass, foot angle, and medial-lateral stability margins were determined. In addition, braking/loading and accelerating/unloading impulses while in contact with the rollers and the rate of loading the rollers were determined from ground reaction forces. Results demonstrate that the reactive recovery response to the first slip consisted of a rapid onset of a flexor synergy (146-199 ms), a large arm elevation strategy, and a modified swing limb trajectory. With repeated exposure to the slip perturbation, the CNS rapidly adapts within one slip trial through global changes. These changes include the attenuation of muscle response magnitude, reduced braking impulse, landing more flat-footed, and elevating the center of mass. Individuals implement a "surfing strategy" while on the rollers when knowledge of the surface condition was available before hand. Furthermore, knowledge of a slip results in a reduced braking impulse and rate of loading, a shift in medial-lateral center of mass closer to the support limb at foot contact on the rollers and a more flat foot landing. In conclusion, prior experience with the perturbations allows subsequent modification and knowledge of the surface condition results in proactive adjustments to safely traverse the slippery surface.
Although the corticospinal tract is not essential for the production of the basic locomotor rhythm in cats, it does contribute to the regulation of locomotion, particularly in situations in which there is a requirement for precise control over paw placement or limb trajectory. Lesions of the dorsolateral funiculi at the low thoracic level (T(13)) that completely interrupted both the cortico- and rubrospinal pathways produced long-term deficits in locomotion on a level surface. These deficits included a paw-drag that was probably caused both by a loss of cortico- and rubrospinal input to motoneurones controlling distal muscles as well as by a change in the relative timing of muscles acting around the hip and knee. Smaller lesions produced similar deficits from which the cats recovered relatively quickly. Cats with the largest lesions of the dorsolateral funiculi were unable to modify their gait sufficiently to step over obstacles attached to the treadmill belt even 3-5 months postlesion. These results imply that the medial pathways, the reticulo- and vestibulospinal pathways, are unable to fully compensate for damage to the lateral pathways. Single unit recordings from identified pyramidal tract neurones (PTNs) within the hindlimb representation of the primary motor cortex (area 4) showed that a substantial proportion of neurones (67%) significantly increased their discharge frequency when the cats modified their gait to step over obstacles attached to the treadmill belt. Of those PTNs that showed increased activity during the swing phase, populations of neurones were activated at different times. A large proportion of PTNS discharged early in swing, in phase with knee flexors such as the semitendinosus. Others discharged slightly later, in phase with the activity of ankle flexors, such as tibialis anterior, while still others discharged at the end of swing, in phase with digit dorsiflexors, such as the extensor digitorum brevis. We suggest that different populations of cortical neurones may specifically modify the activity of selected groups of close synergistic muscles during different parts of the swing phase. We further suggest that these modifications are mediated, in part, by groups of interneurones that are involved in determining the base locomotor rhythm. This provides a means by which the changes specified by the descending signal from the motor cortex may be smoothly, and appropriately, incorporated into the locomotor cycle.
This study examined whether human infants under the age of 12 mo learn to modify their stepping pattern after repeated trip-inducing stimuli. Thirty three infants aged from 5 to 11 mo were studied. The infants were held over a moving treadmill belt to induce stepping. Occasionally, a mechanical tap was applied to the dorsum of the left foot during the early swing phase to elicit a high step. In some trials, the stimulus was applied for only one step. In other trials, the foot was stimulated for a few consecutive steps. We determined whether the infants continued to show high stepping immediately after the removal of the stimuli. The results showed that after the foot was touched for two or more consecutive steps, some infants continued to demonstrate high stepping for a few steps after the removal of the stimuli (i.e., aftereffect). Such adaptation was achieved by an increase in hip and knee flexor muscle torque, which led to greater hip and knee flexion during the early swing phase. Aftereffects were more commonly seen in older infants (9 mo or older). The results indicated that before the onset of independent walking, the locomotor circuitry in human infants is capable of adaptive locomotor plasticity. The increased incidence of aftereffect in older infants also suggests that the ability to adapt to repeated trip-inducing stimuli may be related to other factors such as experience in stepping and maturation of the nervous system.
It is generally accepted that locomotion in mammals, including humans, is based on the activity of neuronal circuits within the spinal cord (the central pattern generator, CPG). Afferent information from the periphery (i.e. the limbs) influences the central pattern and, conversely, the CPG selects appropriate afferent information according to the external requirement. Both the CPG and the reflexes that mediate afferent input to the spinal cord are under the control of the brainstem. There is increasing evidence that in central motor diseases, a defective utilization of afferent input, in combination with secondary compensatory processes, is involved in typical movement disorders, such as spasticity and Parkinson's disease. Recent studies indicate a plastic behavior of the spinal neuronal circuits following a central motor lesion. This has implications for any rehabilitative therapy that should be directed to take advantage of the plasticity of the central nervous system. The significance of this research is in a better understanding of the pathophysiology underlying movement disorders and the consequences for an appropriate treatment.
In the walking system of the cat, feedback from muscle proprioceptors establishes the timing of major phase transitions in the motor pattern, contributes to the production of burst activity, generates some features of the motor pattern, and is required for the adaptive modification of the motor pattern in response to alterations in leg mechanics. How proprioceptive signals are integrated into central neuronal networks has not been fully established, largely due to the absence of detailed information on the functional characteristics of central networks in the presence of phasic afferent signals. Nevertheless, it appears likely that afferent signals reorganize the functioning of central networks, and the concept that the generation of the motor pattern can be explained by afferent modulation of a hard-wired central pattern generator may be too simplistic.