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ABSTRACT: Adolescent idiopathic scoliosis in humans is often associated with vestibulomotor deficits. Compatible with a vestibular origin, scoliotic deformations were provoked in adult Xenopus frogs by unilateral labyrinthectomy (UL) at larval stages. The aquatic ecophysiology and absence of body-weight-supporting limb proprioceptive signals in amphibian tadpoles as a potential sensory substitute after UL might be the cause for a persistent asymmetric descending vestibulospinal activity. Therefore, peripheral vestibular lesions in larval Xenopus were used to reveal the morphophysiological alterations at the cellular and network levels. As a result, spinal motor nerves that were modulated by the previously intact side before UL remained permanently silent during natural vestibular stimulation after the lesion. In addition, retrograde tracing of descending pathways revealed a loss of vestibular neurons on the ipsilesional side with crossed vestibulospinal projections. This loss facilitated a general mass imbalance in descending premotor activity and a permanent asymmetric motor drive to the axial musculature. Therefore, we propose that the persistent asymmetric contraction of trunk muscles exerts a constant, uncompensated differential mechanical pull on bilateral skeletal elements that enforces a distortion of the soft cartilaginous skeletal elements and bone shapes. This ultimately provokes severe scoliotic deformations during ontogenetic development similar to the human syndrome.
Journal of Neuroscience 04/2013; 33(16):6845-56. · 7.11 Impact Factor
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ABSTRACT: In swimming Xenopus laevis tadpoles, gaze stabilization is achieved by efference copies of spinal locomotory CPG output that produce rhythmic extraocular motor activity appropriate for minimizing motion-derived visual disturbances. During metamorphosis, Xenopus switches its locomotory mechanism from larval tail-based undulatory movements to bilaterally synchronous hindlimb kick propulsion in the adult. The change in locomotory mode leads to body motion dynamics that no longer require conjugate left-right eye rotations for effective retinal image stabilization. Using in vivo kinematic analyses, in vitro electrophysiological recordings and specific CNS lesions, we have investigated spino-extraocular motor coupling in the juvenile frog and the underlying neural pathways to understand how gaze control processes are altered in accordance with the animal's change in body plan and locomotor strategy. Recordings of extraocular and limb motor nerves during spontaneous "fictive" swimming in isolated CNS preparations revealed that there is indeed a corresponding change in spinal efference copy control of extraocular motor output. In contrast to fictive larval swimming where alternating bursts occur in bilateral antagonistic horizontal extraocular nerves, during adult fictive limb-kicking, these motor nerves are synchronously active in accordance with the production of convergent eye movements during the linear head accelerations resulting from forward propulsion. Correspondingly, the neural pathways mediating spino-extraocular coupling have switched from contralateral to strictly ipsilateral ascending influences that ensure a coactivation of bilateral extraocular motoneurons with synchronous left-right limb extensions. Thus, adaptive developmental plasticity during metamorphosis enables spinal CPG-driven extraocular motor activity to match the changing requirements for eye movement control during self-motion.
Journal of Neuroscience 03/2013; 33(10):4253-64. · 7.11 Impact Factor
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ABSTRACT: In guiding adaptive behavior, efference copy signals or corollary discharge are traditionally considered to serve as predictors of self-generated sensory inputs and by interfering with their central processing are able to counter unwanted consequences of an animal's own actions. Here, in a speculative reflection on this issue, we consider a different functional role for such intrinsic predictive signaling, namely in stabilizing gaze during locomotion where resultant changes in head orientation in space require online compensatory eye movements in order to prevent retinal image slip. The direct activation of extraocular motoneurons by locomotor-related efference copies offers a prospective substrate for assisting self-motion derived sensory feedback, rather than being subtracted from the sensory signal to eliminate unwanted reafferent information. However, implementing such a feed-forward mechanism would be critically dependent on an appropriate phase coupling between rhythmic propulsive movement and resultant head/visual image displacement. We used video analyzes of actual locomotor behavior and basic theoretical modeling to evaluate head motion during stable locomotion in animals as diverse as Xenopus laevis tadpoles, teleost fish and horses in order to assess the potential suitability of spinal efference copies to the stabilization of gaze during locomotion. In all three species, and therefore regardless of aquatic or terrestrial environment, the head displacements that accompanied locomotor action displayed a strong correlative spatio-temporal relationship in correspondence with a potential predictive value for compensatory eye adjustments. Although spinal central pattern generator-derived efference copies offer appropriately timed commands for extraocular motor control during self-generated motion, it is likely that precise image stabilization requires the additional contributions of sensory feedback signals. Nonetheless, the predictability of the visual consequences of stereotyped locomotion renders intrinsic efference copy signaling an appealing mechanism for offsetting these disturbances, thus questioning the exclusive role traditionally ascribed to sensory-motor transformations in stabilizing gaze during vertebrate locomotion.
Biological Cybernetics 11/2012; · 1.59 Impact Factor
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ABSTRACT: Self-generated body movements require compensatory eye and head adjustments in order to avoid perturbation of visual information processing. Retinal image stabilization is traditionally ascribed to the transformation of visuovestibular signals into appropriate extraocular motor commands for compensatory ocular movements. During locomotion, however, intrinsic "efference copies" of the motor commands deriving from spinal central pattern generator (CPG) activity potentially offer a reliable and rapid mechanism for image stabilization, in addition to the slower contribution of movement-encoding sensory inputs.
Using a variety of in vitro and in vivo preparations of Xenopus tadpoles, we demonstrate that spinal locomotor CPG-derived efference copies do indeed produce effective conjugate eye movements that counteract oppositely directed horizontal head displacements during undulatory tail-based locomotion. The efference copy transmission, by which the extraocular motor system becomes functionally appropriated to the spinal cord, is mediated by direct ascending pathways. Although the impact of the CPG feedforward commands matches the spatiotemporal specificity of classical vestibulo-ocular responses, the two fundamentally different signals do not contribute collectively to image stabilization during swimming. Instead, when the CPG is active, horizontal vestibulo-ocular reflexes resulting from head movements are selectively suppressed.
These results therefore challenge our traditional understanding of how animals offset the disruptive effects of propulsive body movements on visual processing. Specifically, our finding that predictive efference copies of intrinsic, rhythmic neural signals produced by the locomotory CPG supersede, rather than supplement, reactive vestibulo-ocular reflexes in order to drive image-stabilizing eye adjustments during larval frog swimming, represents a hitherto unreported mechanism for vertebrate ocular motor control.
Current biology: CB 07/2012; 22(18):1649-58. · 10.99 Impact Factor
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ABSTRACT: Studies of behavioral consequences after unilateral labyrinthectomy have a long tradition in the quest of determining rules and limitations of the central nervous system (CNS) to exert plastic changes that assist the recuperation from the loss of sensory inputs. Frogs were among the first animal models to illustrate general principles of regenerative capacity and reorganizational neural flexibility after a vestibular lesion. The continuous successful use of the latter animals is in part based on the easy access and identifiability of nerve branches to inner ear organs for surgical intervention, the possibility to employ whole brain preparations for in vitro studies and the limited degree of freedom of postural reflexes for quantification of behavioral impairments and subsequent improvements. Major discoveries that increased the knowledge of post-lesional reactive mechanisms in the CNS include alterations in vestibular commissural signal processing and activation of cooperative changes in excitatory and inhibitory inputs to disfacilitated neurons. Moreover, the observed increase of synaptic efficacy in propriospinal circuits illustrates the importance of limb proprioceptive inputs for postural recovery. Accumulated evidence suggests that the lesion-induced neural plasticity is not a goal-directed process that aims toward a meaningful restoration of vestibular reflexes but rather attempts a survival of those neurons that have lost their excitatory inputs. Accordingly, the reaction mechanism causes an improvement of some components but also a deterioration of other aspects as seen by spatio-temporally inappropriate vestibulo-motor responses, similar to the consequences of plasticity processes in various sensory systems and species. The generality of the findings indicate that frogs continue to form a highly amenable vertebrate model system for exploring molecular and physiological events during cellular and network reorganization after a loss of vestibular function.
Frontiers in neurology. 01/2012; 3:42.
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ABSTRACT: The amphibian Xenopus laevis represents a highly amenable model system for exploring the ontogeny of central neural networks, the functional establishment of sensory-motor transformations, and the generation of effective motor commands for complex behaviors. Specifically, the ability to employ a range of semi-intact and isolated preparations for in vitro morphophysiological experimentation has provided new insights into the developmental and integrative processes associated with the generation of locomotory behavior during changing life styles. In vitro electrophysiological studies have begun to explore the functional assembly, disassembly and dynamic plasticity of spinal pattern generating circuits as Xenopus undergoes the developmental switch from larval tail-based swimming to adult limb-based locomotion. Major advances have also been made in understanding the developmental onset of multisensory signal processing for reactive gaze and posture stabilizing reflexes during self-motion. Additionally, recent evidence from semi-intact animal and isolated CNS experiments has provided compelling evidence that in Xenopus tadpoles, predictive feed-forward signaling from the spinal locomotor pattern generator are engaged in minimizing visual disturbances during tail-based swimming. This new concept questions the traditional view of retinal image stabilization that in vertebrates has been exclusively attributed to sensory-motor transformations of body/head motion-detecting signals. Moreover, changes in visuomotor demands associated with the developmental transition in propulsive strategy from tail- to limb-based locomotion during metamorphosis presumably necessitates corresponding adaptive alterations in the intrinsic spinoextraocular coupling mechanism. Consequently, Xenopus provides a unique opportunity to address basic questions on the developmental dynamics of neural network assembly and sensory-motor computations for vertebrate motor behavior in general.
Developmental Neurobiology 08/2011; 72(4):649-63. · 3.55 Impact Factor
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ABSTRACT: Head motion-related sensory signals are transformed by second-order vestibular neurons (2°VNs) into appropriate commands for retinal image stabilization during body motion. In frogs, these 2°VNs form two distinct subpopulations that have either tonic or highly phasic intrinsic properties, essentially compatible with low-pass and bandpass filter characteristics, respectively. In the present study, physiological data on cellular properties of 2°VNs of the grass frog (Rana temporaria) have been used to construct conductance-based spiking cellular models that were fine-tuned by fitting to recorded spike-frequency data. The results of this approach suggest that low-threshold, voltage-dependent potassium channels in phasic and spike-dependent potassium channels in tonic 2°VNs are important contributors to the differential, yet complementary response characteristics of the two vestibular subtypes. Extension of the cellular model with conductance-based synapses allowed simulation of afferent excitation and evaluation of the emerging properties of local feedforward inhibitory circuits. This approach revealed the relative contributions of intrinsic and synaptic factors on afferent signal processing in phasic 2°VNs. Additional extension of the single-cell model to a population model allowed testing under more natural conditions including asynchronous afferent labyrinthine input and synaptic noise. This latter approach indicated that the feedforward inhibition from the local inhibitory network acts as a high-pass filter, which reinforces the impact of the intrinsic membrane properties of phasic 2°VNs on peak response amplitude and timing. Thus, the combination of cellular and network properties enables phasic 2°VNs to work as a noise-resistant detector, suitable for central processing of short-duration vestibular signals.
Journal of Neuroscience 06/2011; 31(23):8359-72. · 7.11 Impact Factor
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ABSTRACT: Second-order vestibular neurons (2°VN) are the central element for the transformation of body motion-related sensory signals into extraocular motor commands for retinal image stabilization during locomotion. The wide range of motion dynamics necessitates sensory signal transformation in parallel, frequency-tuned channels. Accordingly, in various vertebrates, 2°VN have been shown to form differently tuned functional subgroups. In frog, these neurons subdivide into two separate populations with distinctly different intrinsic membrane properties, discharge dynamics and synaptic response characteristics. Frog tonic 2°VN exhibit low-pass filter characteristics and membrane properties that cause amplification of synaptic inputs, whereas phasic 2°VN form band-pass filters that allow frequency-dependent shunting of repetitive inputs. The differential, yet complementary membrane properties render tonic 2°VN particularly suitable for synaptic integration and phasic 2°VN for differentiation and event detection. Differential insertion of the two cell types into local circuits reinforces the functional consequences of the intrinsic membrane properties, respectively. As a consequence, the synergy of cellular and network properties creates sets of neuronal elements with particular filter characteristics that form flexible, frequency-tuned components for optimal transformation of all dynamic aspects of body motion-related multisensory signals.
Journal of Vestibular Research 01/2011; 21(1):5-19. · 1.35 Impact Factor
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Hans Straka
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ABSTRACT: Vestibulo-ocular reflexes (VOR) assist retinal image stabilization during vertebrate locomotion thereby ensuring accurate visual perception. The importance of this motor behavior for animal survival requires that the underlying circuitry and all individual components are fully developed and functional as soon as post-embryonic animals initiate self-motion. Recent progress on the genetic, molecular, and activity-dependent regulation of placode development, vestibular sensory organ formation, circuit assembly, and acquisition of neuronal properties revealed rules and restrictions that give insight into how hindbrain VOR neuronal networks are assembled and become functional during ontogeny. Major crucial steps that correlate with early/delayed functional VOR onsets concern the maturation of cellular properties (precocial/altricial species) and the acquisition of minimal semicircular canal dimensions (small-sized vertebrates).
Current opinion in neurobiology 12/2010; 20(6):689-95. · 7.21 Impact Factor
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ABSTRACT: Central vestibular neurons receive substantial inputs from the contralateral labyrinth through inhibitory and excitatory brainstem commissural pathways. The functional organization of these pathways was studied by a multi-methodological approach in isolated frog whole brains. Retrogradely labeled vestibular commissural neurons were primarily located in the superior vestibular nucleus in rhombomeres 2/3 and the medial and descending vestibular nucleus in rhombomeres 5-7. Restricted projections to contralateral vestibular areas, without collaterals to other classical vestibular targets, indicate that vestibular commissural neurons form a feedforward push-pull circuitry. Electrical stimulation of the contralateral coplanar semicircular canal nerve evoked in canal-related second-order vestibular neurons (2 degrees VN) commissural IPSPs (approximately 70%) and EPSPs (approximately 30%) with mainly (approximately 70%) disynaptic onset latencies. The dynamics of commissural responses to electrical pulse trains suggests mediation predominantly by tonic vestibular neurons that activate in all tonic 2 degrees VN large-amplitude IPSPs with a reversal potential of -74 mV. In contrast, phasic 2 degrees VN exhibited either nonreversible, small-amplitude IPSPs (approximately 40%) of likely dendritic origin or large-amplitude commissural EPSPs (approximately 60%). IPSPs with disynaptic onset latencies were exclusively GABAergic (mainly GABA(A) receptor-mediated) but not glycinergic, compatible with the presence of GABA-immunopositive (approximately 20%) and the absence of glycine-immunopositive vestibular commissural neurons. In contrast, IPSPs with longer, oligosynaptic onset latencies were GABAergic and glycinergic, indicating that both pharmacological types of local inhibitory neurons were activated by excitatory commissural fibers. Conservation of major morpho-physiological and pharmacological features of the vestibular commissural pathway suggests that this phylogenetically old circuitry plays an essential role for the processing of bilateral angular head acceleration signals in vertebrates.
Journal of Neuroscience 03/2010; 30(9):3310-25. · 7.11 Impact Factor
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ABSTRACT: Human idiopathic scoliosis is characterized by severe deformations of the spine and skeleton. The occurrence of vestibular-related deficits in these patients is well established but it is unclear whether a vestibular pathology is the common cause for the scoliotic syndrome and the gaze/posture deficits or if the latter behavioral deficits are a consequence of the scoliotic deformations. A possible vestibular origin was tested in the frog Xenopus laevis by unilateral removal of the labyrinthine endorgans at larval stages. After metamorphosis into young adult frogs, X-ray images and three-dimensional reconstructed micro-computer tomographic scans of the skeleton showed deformations similar to those of scoliotic patients. The skeletal distortions consisted of a curvature of the spine in the frontal and sagittal plane, a transverse rotation along the body axis and substantial deformations of all vertebrae. In terrestrial vertebrates, the initial postural syndrome after unilateral labyrinthectomy recovers over time and requires body weight-supporting limb proprioceptive information. In an aquatic environment, however, this information is absent. Hence, the lesion-induced asymmetric activity in descending spinal pathways and the resulting asymmetric muscular tonus persists. As a consequence the mostly cartilaginous skeleton of the frog tadpoles progressively deforms. Lack of limb proprioceptive signals in an aquatic environment is thus the element, which links the Xenopus model with human scoliosis because a comparable situation occurs during gestation in utero. A permanently imbalanced activity in descending locomotor/posture control pathways might be the common origin for the observed structural and behavioral deficits in humans as in the different animal models of scoliosis.
Journal of Neuroscience 10/2009; 29(40):12477-83. · 7.11 Impact Factor
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ABSTRACT: Computational modeling of cellular and network properties of central vestibular neurons is necessary for understanding the mechanisms of sensory-motor transformation for gaze stabilization. As a first step to mathematically describe vestibular signal processing, the available physiological data of the synaptic and intrinsic properties of frog second-order vestibular neurons (2 degrees VN) were used to create a model that combines cellular and network parameters. With this approach it is now possible to reveal the particular contributions of intrinsic membrane versus emerging network properties in shaping labyrinthine afferent-evoked synaptic responses in 2 degrees VN, to simulate perturbations, and to generate hypotheses that are testable in empiric experiments.
Annals of the New York Academy of Sciences 06/2009; 1164:451-4. · 3.15 Impact Factor
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ABSTRACT: Self-generated locomotor activity is accompanied by head movements that cause retinal image displacements with a resultant degradation of visual information processing. To maintain visual acuity, retinal image drift must be counteracted by dynamic compensatory gaze adjustments that derive to a large extent from vestibulo-ocular reflexes (VOR). During head motion, vestibular signals code a wide frequency range from static head position to high acceleration profiles during rapid head turns. This large dynamic range suggests that the sensory-motor transformation occurs in parallel, yet complementary frequency-tuned pathways. In fact, the classic "three-neuronal" VOR pathway is composed of distinct functional subgroups of cells with different intrinsic properties and response dynamics at each synaptic level. This generates sets of neuronal filters that are ideal for particular frequency ranges and signaling patterns, respectively. In second-order vestibular subgroups, different filter functions, and hence a different synaptic processing is facilitated by a coadaptation of intrinsic membrane and emerging network properties. The consecutive assembly and sequential connectivity of pre- and postsynaptic neuronal elements with corresponding physiological properties, generates parallel pathways that allow for separate coding of different dynamic head-motion components during locomotor activity.
Annals of the New York Academy of Sciences 06/2009; 1164:37-44. · 3.15 Impact Factor
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BMC Neuroscience. 01/2009;
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ABSTRACT: Intrinsic cellular properties of neurons in culture or slices are usually studied by the whole cell clamp method using low-resistant patch pipettes. These electrodes allow detailed analyses with standard electrophysiological methods such as current- or voltage-clamp. However, in these preparations large parts of the network and dendritic structures may be removed, thus preventing an adequate study of synaptic signal processing. Therefore, intact in vivo preparations or isolated in vitro whole brains have been used in which intracellular recordings are usually made with sharp, high-resistant electrodes to optimize the impalement of neurons. The general non-linear resistance properties of these electrodes, however, severely limit accurate quantitative studies of membrane dynamics especially needed for precise modelling. Therefore, we have developed a frequency-domain analysis of membrane properties that uses a Piece-wise Non-linear Electrode Compensation (PNEC) method. The technique was tested in second-order vestibular neurons and abducens motoneurons of isolated frog whole brain preparations using sharp potassium chloride- or potassium acetate-filled electrodes. All recordings were performed without online electrode compensation. The properties of each electrode were determined separately after the neuronal recordings and were used in the frequency-domain analysis of the combined measurement of electrode and cell. This allowed detailed analysis of membrane properties in the frequency-domain with high-resistant electrodes and provided quantitative data that can be further used to model channel kinetics. Thus, sharp electrodes can be used for the characterization of intrinsic properties and synaptic inputs of neurons in intact brains.
Frontiers in Neuroscience 01/2009; 3:64.
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ABSTRACT: The sensory-motor transformation of the large dynamic spectrum of head-motion-related signals occurs in separate vestibulo-ocular pathways. Synaptic responses of tonic and phasic second-order vestibular neurons were recorded in isolated frog brains after stimulation of individual labyrinthine nerve branches with trains of single electrical pulses. The timing of the single pulses was adapted from spike discharge patterns of frog semicircular canal nerve afferents during sinusoidal head rotation. Because each electrical pulse evoked a single spike in afferent fibers, the resulting sequences with sinusoidally modulated intervals and peak frequencies up to 100 Hz allowed studying the processing of presynaptic afferent inputs with in vivo characteristics in second-order vestibular neurons recorded in vitro in an isolated whole brain. Variation of pulse-train parameters showed that the postsynaptic compound response dynamics differ in the two types of frog vestibular neurons. In tonic neurons, subthreshold compound responses and evoked discharge patterns exhibited relatively linear dynamics and were generally aligned with pulse frequency modulation. In contrast, compound responses of phasic neurons were asymmetric with large leads of subthreshold response peaks and evoked spike discharge relative to stimulus waveform. These nonlinearities were caused by the particular intrinsic properties of phasic vestibular neurons and were facilitated by GABAergic and glycinergic inhibitory inputs from tonic type vestibular interneurons and by cerebellar circuits. Coadapted intrinsic filter and emerging network properties thus form dynamically different neuronal elements that provide the appropriate cellular basis for a parallel processing of linear, tonic, and nonlinear phasic vestibulo-ocular response components in central vestibular neurons.
Journal of Neuroscience 11/2008; 28(41):10349-62. · 7.11 Impact Factor
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ABSTRACT: Semicircular canals have been sensors of angular acceleration for 450 million years. This vertebrate adaptation enhances survival by implementing postural and visual stabilization during motion in a three-dimensional environment. We used an integrated neuroethological approach in larval Xenopus to demonstrate that semicircular canal dimensions, and not the function of other elements, determines the onset of angular acceleration detection. Before angular vestibuloocular function in either the vertical or horizontal planes, at stages 47 and 48, respectively, each individual component of the vestibuloocular system was shown to be operational: extraocular muscles could be activated, central neural pathways were complete, and canal hair cells were capable of evoking graded responses. For Xenopus, a minimum semicircular canal lumen radius of 60 microm was necessary to permit endolymph displacement sufficient for sensor function at peak accelerations of 400 degrees /s(2). An intra-animal comparison demonstrated that this size is reached in the vertical canals earlier in development than in the horizontal canals, corresponding to the earlier onset of vertical canal-activated ocular motor behavior. Because size constitutes a biophysical threshold for canal-evoked behavior in other vertebrates, such as zebrafish, we suggest that the semicircular canal lumen and canal circuit radius are limiting the onset of vestibular function in all small vertebrates. Given that the onset of gravitoinertial acceleration detection precedes angular acceleration detection by up to 10 d in Xenopus, these results question how the known precise spatial patterning of utricular and canal afferents in adults is achieved during development.
Journal of Neuroscience 09/2008; 28(32):8086-95. · 7.11 Impact Factor
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ABSTRACT: Labyrinthine nerve-evoked monosynaptic excitatory postsynaptic potentials (EPSPs) in second-order vestibular neurons (2 degrees VN) sum with disynaptic inhibitory postsynaptic potentials (IPSPs) that originate from the thickest afferent fibers of the same nerve branch and are mediated by neurons in the ipsilateral vestibular nucleus. Pharmacological properties of the inhibition and the interaction with the afferent excitation were studied by recording monosynaptic responses of phasic and tonic 2 degrees VN in an isolated frog brain after electrical stimulation of individual semicircular canal nerves. Specific transmitter antagonists revealed glycine and GABA(A) receptor-mediated IPSPs with a disynaptic onset only in phasic but not in tonic 2 degrees VN. Compared with GABAergic IPSPs, glycinergic responses in phasic 2 degrees VN have larger amplitudes and a longer duration and reduce early and late components of the afferent nerve-evoked subthreshold activation and spike discharge. The difference in profile of the disynaptic glycinergic and GABAergic inhibition is compatible with the larger number of glycinergic as opposed to GABAergic terminal-like structures on 2 degrees VN. The increase in monosynaptic excitation after a block of the disynaptic inhibition in phasic 2 degrees VN is in part mediated by a N-methyl-d-aspartate receptor-activated component. Although inhibitory inputs were superimposed on monosynaptic EPSPs in tonic 2 degrees VN as well, the much longer latency of these IPSPs excludes a control by short-latency inhibitory feed-forward side-loops as observed in phasic 2 degrees VN. The differential synaptic organization of the inhibitory control of labyrinthine afferent signals in phasic and tonic 2 degrees VN is consistent with the different intrinsic signal processing modes of the two neuronal types and suggests a co-adaptation of intrinsic membrane properties and emerging network properties.
Journal of Neurophysiology 05/2008; 99(4):1758-69. · 3.32 Impact Factor
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Current Biology 04/2008; 18(6):R241-3. · 9.65 Impact Factor
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ABSTRACT: Central vestibular neurons process head movement-related sensory signals over a wide dynamic range. In the isolated frog whole brain, second-order vestibular neurons were identified by monosynaptic responses after electrical stimulation of individual semicircular canal nerve branches. Neurons were classified as tonic or phasic vestibular neurons based on their different discharge patterns in response to positive current steps. With increasing frequency of sinusoidally modulated current injections, up to 100 Hz, there was a concomitant decrease in the impedance of tonic vestibular neurons. Subthreshold responses as well as spike discharge showed classical low-pass filter-like characteristics with corner frequencies ranging from 5 to 20 Hz. In contrast, the impedance of phasic vestibular neurons was relatively constant over a wider range of frequencies or showed a resonance at approximately 40 Hz. Above spike threshold, single spikes of phasic neurons were synchronized with the sinusoidal stimulation between approximately 20 and 50 Hz, thus showing characteristic bandpass filter-like properties. Both the subthreshold resonance and bandpass filter-like discharge pattern depend on the activation of an I(D) potassium conductance. External current or synaptic stimulation that produced impedance increases (i.e., depolarization in tonic or hyperpolarization in phasic neurons) had opposite and complementary effects on the responses of the two types of neurons. Thus, membrane depolarization by current steps or repetitive synaptic excitation amplified synaptic inputs in tonic vestibular neurons and reduced them in phasic neurons. These differential, opposite membrane response properties render the two neuronal types particularly suitable for either integration (tonic neurons) or signal detection (phasic neurons), respectively, and dampens variations of the resting membrane potential in the latter.
Journal of Neuroscience 05/2007; 27(16):4283-96. · 7.11 Impact Factor
