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Understanding motor events: A neurophysiological study
Abstract
Neurons of the rostral part of inferior premotor cortex of the monkey discharge during goal-directed hand movements such as grasping, holding, and tearing. We report here that many of these neurons become active also when the monkey observes specific, meaningful hand movements performed by the experimenters. The effective experimenters' movements include among others placing or retrieving a piece of food from a table, grasping food from another experimenter's hand, and manipulating objects. There is always a clear link between the effective observed movement and that executed by the monkey and, often, only movements of the experimenter identical to those controlled by a given neuron are able to activate it. These findings indicate that premotor neurons can retrieve movements not only on the basis of stimulus characteristics, as previously described, but also on the basis of the meaning of the observed actions.
... In fact, mirror neurons discharge when an object-directed action is performed but also when an action is perceived (Rizzolatti and Craighero, 2004;van der Wel et al., 2013). A variety of studies investigated the role of mirror neurons in parieto-frontal circuits in monkeys (Bonini et al., 2010;Caggiano et al., 2009;Di Pellegrino et al., 1992;Gallese et al., 1996;Rizzolatti and Sinigaglia, 2010) and humans (Iacoboni et al., 2005;Mukamel et al., 2010). In particular, the mirror neuron system can be referred to as two principal hubs: the frontal lobe and the IPL. ...
... In particular, the mirror neuron system can be referred to as two principal hubs: the frontal lobe and the IPL. This type of neuron was first discovered in area F5 of the ventral premotor cortex of macaques (Di Pellegrino et al., 1992;Gallese et al., 1996;Rizzolatti et al., 1997), where neurons that are responsive to the presentation of an object as the monkey grasps it are also present (Murata et al., 1997;Raos et al., 2006). Area F5 is active during both the observation and execution of specific goal-directed actions involving the hand and the mouth (Ferri et al., 2015) due to the coexistence of motor and mirror neurons. ...
... This means that most V6A cells easily discriminate one's own actions from the actions of others. A small subset of V6A neurons (20%) discharge during both grasp execution and the observation of another's grasping, apparently complying with the original definition of mirror neurons (di Pellegrino et al., 1992;Gallese et al., 1996;Rizzolatti et al., 1997). It must however be highlighted that the incidence of mirror neurons in V6A is much lower than in the IPL or in ventral premotor cortex. ...
... In the last few decades, cognitive neuroscience shed light on the underlying dynamics of this type of empathic resonance. Evidence shows that humans and other animalslikely including dogs too (Sue 2016), are empathic beings equipped with mirror neurons, a specific type of neurons that reproduce in the bodymind of an observer what is being observed in the actions of others (Gazzola et al. 2006;Heimann et al. 2014;Kohler (toward) a canine anthropology Pellegrino et al. 1992;Rizzolatti et al. 1988;Rizzolatti and Sinigaglia 2010;Rochat et al. 2010). Based on those relevant findings, theatre scholars further investigated the convergence of cognitive neuroscience, theatre and the synaesthetic exchange between the actor and the spectator (Falletti et al. 2016). ...
Understanding dog and human interaction in all forms is essential to improve the relationship between the two species and further contribute to a fair process of mutual influence. That is fundamental for dog parents/caregivers/ guardians and professionals working with dogs and people at any level. Additionally, dog-human communication, behaviour and training may play a critical role in rediscussing human supremacy, for people follow dog behaviour and training models extensively and worldwide.
Countless studies on dog behaviour and cognition have unfolded excellent knowledge in recent decades. However, the psychophysical interface of dog-human interaction needs to be explored further. To investigate this aspect with a multidisciplinary approach, I gather elements from Theatre Anthropology, psychophysiology, cognitive neuroscience and bodymind practices. I introduce the theoretical frame of Canine Anthropology to focus on the psychophysicality of the human bodymind and its canine counterpart when some interactions between the two species occur. I describe the roles of the human “actor” and the canine “spectator” involved in complex events that generate meaning. A human's body position, action, and intention critically impact dog behaviour, and the dog-human interaction acquires a phenomenological significance. As spectators and mediators, dogs can affect human behaviour and flip their roles. They are the receivers and the reciprocators of human synaesthetic transmission. Thus, the dog-human interaction discloses itself as a psychophysical and embodied experience.
... One functional network potentially associated with the processing of observed pain is the mirror neuron system (MNS). The MNS is a network in the brain believed to contain mirror neurons, which activate not only when an action is performed but also when it is observed [12][13][14]. While the primary functions attributed to the MNS in social cognition are action understanding and imitation [15], a significant body of literature supports its involvement in empathy. ...
Aim: The aim of this study is to analyze the brain activity patterns during the observation of painful expressions and to establish the relationship between this activity and the scores obtained on the Interpersonal Reactivity Index (IRI). Methods: The study included twenty healthy, right-handed subjects (10 women). We conducted a task-based and resting-state functional magnetic resonance imaging (fMRI) study. The task involved observing pictures displaying painful expressions. We performed a region of interest (ROI) analysis focusing on the core regions of the sensorimotor mirror neuron system (MNS). Resting-state fMRI was utilized to assess the functional connectivity of the sensorimotor MNS regions with the rest of the cortex using a seed-to-voxel approach. Additionally, we conducted a regression analysis to examine the relationship between brain activity and scores from the IRI subtests. Results: Observing painful expressions led to increased activity in specific regions of the frontal, temporal, and parietal lobes. The largest cluster of activation was observed in the left inferior parietal lobule (IPL). However, the ROI analysis did not reveal any significant activity in the remaining core regions of the sensorimotor MNS. The regression analysis demonstrated a positive correlation between brain activity during the observation of pain and the “empathic concern” subtest scores of the IRI in both the cingulate gyri and bilateral IPL. Finally, we identified a positive relationship between the “empathic concern” subtest of the IRI and the functional connectivity (FC) of bilateral IPLs with the bilateral prefrontal cortex and the right IFG. Conclusion: Observing expressions of pain triggers activation in the sensorimotor MNS, and this activation is influenced by the individual’s level of empathy.
... The opportunity for learners to observe their partner in the dyad has been suggested to be the primary variable facilitating skill acquisition in dyad practice. The processes underlying action execution and action observation are thought to be mediated by a common neural network involving the mirror neuron system which is proposed to be the neurophysiological basis for observational learning (Di Pellegrino et al., 1992). The mirror neurons are a specialized class of premotor neurons that become activated when observing and performing a goal-directed action, such as grasping. ...
... The mirror neuron system (MNS) entails the activity of the neuron population that is activated both when an individual performs a specific action and when individuals observe a similar action performed by another individual. Mirror neurons were first discovered in ventral premotor area F5 of the macaque monkey [1]. They were also shown to exist in a region of the inferior parietal lobule [2]. ...
Background/aim: The firing rate of the mirror neuron system in monkeys decreases systematically with more repetitions. The aim of
this study is to investigate whether the activity of the mirror neuron system varies based on the observed movement and the contents
of the action, as well as whether there is inhibition in the mirror neuron system when humans observe repeated actions. If inhibition is
present, the second question of the study is whether it is related to the organization of the observed action.
Materials and methods: Fourteen healthy volunteers participated in the study. Transcranial magnetic stimulation was applied to the left
primary motor cortex and motor evoked potentials (MEPs) were recorded from the right first dorsal interosseous and abductor pollicis
brevis muscles while the participants were watching videos specially prepared for the study.
Results: There were no significant changes in MEP amplitudes compared to baseline MEPs while observing aimless action. However,
while participants watched the repeated action video, the mean MEP amplitude increased at the beginning of the movement, but neither
facilitation nor inhibition was detected when the participants watched the phase of grasping the object of the action compared to the
baseline MEP amplitude. On the other hand, while participants were watching different activities, an increased MEP amplitude was observed
at the beginning of the movement and in the grasping of the object of the action. Additionally, there was no significant reduction
in MEP amplitude during any movement stages while observing the repeated action video.
Conclusion: The findings of this study suggest that the activation of the mirror neuron system in humans depends on the content and
stages of the observed movement. Additionally, there was no inhibition or systematic reduction in MEP amplitudes while watching a
repeated action.
... This F5 ROI included all three subdivisions of F5-F5p and F5a at different anterior-posterior positions in the posterior bank of the inferior arcuate sulcus and F5c on the adjacent cortical convexity [27][28][29]. Single-cell investigations have demonstrated mirror neurons in each of these ROIs [26,[30][31][32][33][34]. Additionally, each of these regions has been previously shown to yield cross-modal action-specific representations for the same observed and executed reach-and-grasp or reach-and-touch actions [1] used in the current study. ...
To probe the presence of mirror neurons in the human brain, cross-modal fMRI adaptation has been suggested as a suitable technique. The rationale behind this suggestion is that this technique allows making more accurate inferences about neural response properties underlying fMRI voxel activations, beyond merely showing shared voxels that are active during both action observation and execution. However, the validity of using cross-modal fMRI adaptation to demonstrate the presence of mirror neurons in parietal and premotor brain regions has been questioned given the inconsistent and weak results obtained in human studies. A better understanding of cross-modal fMRI adaptation effects in the macaque brain is required as the rationale for using this approach is based on several assumptions related to macaque mirror neuron response properties that still need validation. Here, we conducted a cross-modal fMRI adaptation study in macaque monkeys, using the same action execution and action observation tasks that successfully yielded mirror neuron region cross-modal action decoding in a previous monkey MVPA study. We scanned two male rhesus monkeys while they first executed a sequence of either reach-and-grasp or reach-and-touch hand actions and then observed a video of a human actor performing these motor acts. Both whole-brain and region-of-interest analyses failed to demonstrate cross-modal fMRI adaptation effects in parietal and premotor mirror neuron regions. Our results, in line with previous findings in non-human primates, show that cross-modal motor-to-visual fMRI adaptation is not easily detected in monkey brain regions known to house mirror neurons. Thus, our results advocate caution in using cross-modal fMRI adaptation as a method to infer whether mirror neurons can be found in the primate brain.
The notion of a neuron that responds selectively to the image of a particular complex object has been controversial ever since Gross and his colleagues reported neurons in the temporal cortex of monkeys that were selective for the sight of a monkey's hand (Gross, Rocha-Miranda, & Bender, 1972). Since that time, evidence has mounted for neurons in the temporal lobe that respond selectively to faces. The present paper presents a critical analysis of the evidence for face neurons and discusses the implications of these neurons for models of object recognition. The paper also presents some possible reasons for the evolution of face neurons and suggests some analogies with the development of language in humans.
It has been proposed that the premotor cortex plays a role in the selection of motor programs based on environmental context. To test this hypothesis, we recorded the activity of single neurons as monkeys learned visuomotor associations. The hypothesis predicts that task-related premotor cortical activity before learning should differ from that afterward. We found that a substantial population of premotor cortex neurons, over half of those adequately tested, showed the predicted learning-dependent changes in activity. The present findings support a role for premotor cortex in motor preparation, generally, and suggest a specific role in the selection of movements on the basis of arbitrary associations.
A variety of cell types exist in the temporal cortex providing high-level visual descriptions of bodies and their movements. We have investigated the sensitivity of such cells to different viewing conditions to determine the frame(s) of reference utilized in processing. The responses of the majority of cells in the upper bank of the superior temporal sulcus (areas TPO and PGa) found to be sensitive to static and dynamic information about the body were selective for one perspective view (e.g. right profile, reaching right or walking left). These cells can be considered to provide viewer-centred descriptions because they depend on the observer's vantage point. Viewer-centred descriptions could be used in guiding behaviour. They could also be used as an intermediate step for establishing view-independent responses of other cell types which responded to many or all perspective views selectively of the same object (e.g. head) or movement. These cells have the properties of object-centred descriptions, where the object viewed provides the frame of reference for describing the disposition of object parts and movements (e.g. head on top of shoulders, reaching across the body, walking forward 'following the nose'). For some cells in the lower bank of the superior temporal sulcus (area TEa) the responses to body movements were related to the object or goal of the movements (e.g. reaching for or walking towards a specific place). This goal-centred sensitivity to interaction allowed the cells to be selectively activated in situations where human subjects would attribute causal and intentional relationships.
In four macaque monkeys horseradish peroxidase (HRP) was injected into physiologically defined hand-arm motor area. Ipsilaterally, HRP labeled neurons were found in both upper and lower limbs of the posterior bank of the arcuate sulcus and in an area surrounding the arcuate spur. Contralaterally, labeled neurons were found in the same areas, though less dense in concentration. Labeled neurons were found mostly in layer III of the cortex.
Rhesus monkeys with selective lesions of the frontal cortex were tested on a motor conditional associative-learning task. Monkeys with lesions of the periarcuate area were severely impaired in acquiring this task, whilst monkeys with lesions of the principalis region showed only a mild retardation in learning.
Single neurons were recorded from the rostral part of the agranular frontal cortex (area 6a beta) in awake, partially restrained macaque monkeys. In the medialmost and mesial sectors of this area, rostral to the supplementary motor area, neurons were found which were activated during arm reaching-grasping movements. These neurons ("reaching-grasping neurons") did not appear to be influenced by how the objects were grasped nor, with some exceptions, by where they were located. Their activity changed largely prior to the arm movement and continued until the end of it. The premovement modulation (excitatory or inhibitory) could start with stimulus presentation, with the saccade triggered by the stimulus or after stimulus fixation. The distance of the stimulus from the monkey was an important variable for activating many neurons. About half of the recorded neurons showed a modulation of the same sign during movement and premovement period. The other half showed an increase/decrease in activity which was of the opposite sign during movement and premovement period or part of it. In this last case the discharge changes were of the same sign when the stimulus was close to the monkey and when the monkey moved its arm to reach the objects, whereas they were of opposite sign when the stimulus was outside the animal's reach. Microstimulation of area 6a beta and the reconstruction of the locations of eye movement and arm movement related cells showed that the arm field was located more medially (and mesially) than the eye field described by Schlag and Schlag-Rey (1987). It is suggested that, unlike inferior area 6, which is mostly involved in selection of effectors on the basis of the physical properties of the objects and their spatial location (Rizzolatti and Gentilucci 1988), area 6a beta plays a role in the preparation of reaching-grasping arm movements and in their release when the appropriate conditions are set.
The laminar pattern of cytochrome oxidase activity was studied in the agranular frontal cortex (area 4-6 complex) of the macaque monkey. The cortex, stained with this method, showed 6 stripes of different enzymatic activity. On the basis of their characteristics and of the presence of highly active cells, the agranular frontal cortex could be parcellated in 5 areas (F1-F5). F1 very likely corresponds to area FA of von Bonin and Bailey. Rostral to F1 two large regions could be distinguished, one located medial to the spur of the arcuate sulcus and its imaginary caudal extension, the other laterally. The superior region was formed by areas F2 and F3. The first was located on the dorsomedial cortical surface, the other on the mesial surface. F3 possibly corresponds to the supplementary motor area. The inferior region was formed by areas F4 and F5. The rostral area (F5) showed transition characteristics that rendered it somehow similar to the prefrontal areas. It may correspond to the cytoarchitectonic area FCBm. The cytocrome oxidase technique is a useful means of parcellating the agranular frontal cortex and may greatly help in physiological and behavioral experiments.
Many cells in premotor cortex change their activity while a monkey waits before responding. In the present experiment lesions were placed in premotor cortex in order to investigate the information carried by this neuronal activity. The monkeys were trained to make one of two movements depending on the colour of a cue. There were two conditions: in one they could respond when the cue was presented, in the other they had to wait three seconds before responding. The monkeys were then retested after the bilateral removal of premotor cortex. Animals with premotor lesions performed very poorly under both conditions. It is concluded that premotor cortex is concerned with retrieving the response that is appropriate given a particular cue.