Response of vestibular nerve afferents innervating utricle and saccule during passive and active translations.

The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self- or externally generated.

[1]  R. Gacek,et al.  The localization of vestibular efferent neurons in the kitten with horseradish peroxidase. , 1974, Acta oto-laryngologica.

[2]  J. Goldberg,et al.  The vestibular nerve of the chinchilla. IV. Discharge properties of utricular afferents. , 1990, Journal of neurophysiology.

[3]  S G Lisberger,et al.  Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. , 1976, Journal of neurophysiology.

[5]  D E Angelaki,et al.  Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. , 2000, Journal of neurophysiology.

[6]  Responses to somatosensory input by afferent and efferent neurons in the vestibular nerve of the frog. , 1984, Brain, behavior and evolution.

[7]  Jefferson E. Roy,et al.  Selective Processing of Vestibular Reafference during Self-Generated Head Motion , 2001, The Journal of Neuroscience.

[8]  D. L. Tomko,et al.  Raesponses to head tilt in cat eighth nerve afferents , 1981, Experimental Brain Research.

[9]  J. Goldberg,et al.  Reflections of efferent activity in rotational responses of chinchilla vestibular afferents. , 2002, Journal of neurophysiology.

[10]  R. Baker,et al.  Action of the efferent vestibular system on primary afferents in the toadfish, Opsanus tau. , 1985, Journal of neurophysiology.

[11]  R. Klinke,et al.  Efferent influence on the vestibular organ during active movements of the body , 2004, Pflügers Archiv.

[12]  Curtis C Bell,et al.  The mormyromast region of the mormyrid electrosensory lobe. I. Responses to corollary discharge and electrosensory stimuli. , 2003, Journal of neurophysiology.

[13]  J. Goldberg,et al.  Efferent Actions in the Chinchilla Vestibular Labyrinth , 2004, Journal of the Association for Research in Otolaryngology.

[14]  N. Henriksson,et al.  EFFERENT AND AFFERENT ACTIVITY PATTERN IN THE VESTIBULAR NERVE OF THE FROG. , 1963, Acta oto-laryngologica. Supplementum.

[15]  Dora E. Angelaki,et al.  Sensory Convergence Solves a Motion Ambiguity Problem , 2005, Current Biology.

[16]  R. Tomlinson,et al.  Behavior of cells without eye movement sensitivity in the vestibular nuclei during combined rotational and translational stimuli. , 1996, Journal of vestibular research : equilibrium & orientation.

[17]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. II. Directional selectivity and force-response relations. , 1976, Journal of neurophysiology.

[18]  Jefferson E. Roy,et al.  Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei , 2004, The Journal of Neuroscience.

[19]  G. DeAngelis,et al.  A functional link between area MSTd and heading perception based on vestibular signals , 2007, Nature Neuroscience.

[20]  T. Hirvonen,et al.  Effects of intratympanic gentamicin on vestibular afferents and hair cells in the chinchilla. , 2005, Journal of neurophysiology.

[21]  R. Tomlinson,et al.  Behavior of eye-movement-related cells in the vestibular nuclei during combined rotational and translational stimuli. , 1996, Journal of neurophysiology.

[22]  Daniel M. Wolpert,et al.  The Cerebellum Contributes to Somatosensory Cortical Activity during Self-Produced Tactile Stimulation , 1999, NeuroImage.

[23]  J. Goldberg,et al.  Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey. , 1984, Journal of neurophysiology.

[24]  R. Klinke,et al.  Efferent activity in the goldfish vestibular nerve and its influence on afferent activity , 1980, Pflügers Archiv.

[25]  A. Perachio,et al.  Responses of gerbil utricular afferents to translational motion , 2003, Experimental Brain Research.

[26]  Y. Uchino,et al.  Otolith and canal integration on single vestibular neurons in cats , 2005, Experimental Brain Research.

[27]  Dora E. Angelaki,et al.  Response properties of pigeon otolith afferents to linear acceleration , 1997, Experimental Brain Research.

[28]  H. Straka,et al.  Location of dye-coupled second order and of efferent vestibular neurons labeled from individual semicircular canal or otolith organs in the frog , 2001, Brain Research.

[29]  A. Perachio,et al.  Three-dimensional analysis of vestibular efferent neurons innervating semicircular canals of the gerbil. , 1997, Journal of neurophysiology.

[30]  I S Curthoys,et al.  Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation. , 1971, Brain research.

[31]  Nathaniel B Sawtell,et al.  Central Control of Dendritic Spikes Shapes the Responses of Purkinje-Like Cells through Spike Timing-Dependent Synaptic Plasticity , 2007, The Journal of Neuroscience.

[32]  J. Kaltenbach,et al.  Efferent neurons and vestibular cross talk in the frog. , 1997, Journal of neurophysiology.

[33]  Y. Uchino,et al.  Convergence of the horizontal semicircular canal and otolith afferents on cat single vestibular neurons , 2001, Experimental Brain Research.

[34]  J. Goldberg,et al.  Efferent-Mediated Fluctuations in Vestibular Nerve Discharge: A Novel, Positive-Feedback Mechanism of Efferent Control , 2006, Journal of the Association for Research in Otolaryngology.

[35]  Kathleen E Cullen,et al.  Response of vestibular-nerve afferents to active and passive rotations under normal conditions and after unilateral labyrinthectomy. , 2007, Journal of neurophysiology.

[36]  I. Curthoys,et al.  Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. II. Electrical stimulation. , 1971, Brain research.

[37]  S. Lisberger,et al.  Transformation of vestibular signals into motor commands in the vestibuloocular reflex pathways of monkeys. , 2006, Journal of neurophysiology.

[38]  R. Boyle,et al.  Efferent vestibular system in the toadfish: action upon horizontal semicircular canal afferents , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[39]  L. Harris,et al.  Visual and non-visual cues in the perception of linear self motion , 2000, Experimental Brain Research.

[40]  Y. Uchino,et al.  Convergence patterns of the posterior semicircular canal and utricular inputs in single vestibular neurons in cats , 2000, Experimental Brain Research.

[41]  W. Abend,et al.  Response to static tilts of peripheral neurons innervating otolith organs of the squirrel monkey. , 1972, Journal of neurophysiology.

[42]  A A Perachio,et al.  Convergent properties of vestibular-related brain stem neurons in the gerbil. , 2000, Journal of neurophysiology.

[43]  G T Gdowski,et al.  Firing behavior of vestibular neurons during active and passive head movements: vestibulo-spinal and other non-eye-movement related neurons. , 1999, Journal of neurophysiology.

[44]  Lindeman Hh.  Studies on the morphology of the sensory regions of the vestibular apparatus with 45 figures. , 1969 .

[45]  D. Wolpert,et al.  Central cancellation of self-produced tickle sensation , 1998, Nature Neuroscience.

[46]  Dora E Angelaki,et al.  Vestibular convergence patterns in vestibular nuclei neurons of alert primates. , 2002, Journal of neurophysiology.

[47]  J. Goldberg,et al.  Efferent vestibular system in the squirrel monkey: anatomical location and influence on afferent activity. , 1980, Journal of neurophysiology.

[48]  J. Goldberg,et al.  Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. , 1976, Journal of neurophysiology.

[49]  K. Cullen,et al.  Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey. , 2002, Journal of neurophysiology.

[50]  D E Angelaki,et al.  Role of irregular otolith afferents in the steady-state nystagmus during off-vertical axis rotation. , 1992, Journal of neurophysiology.

[51]  M. Sommer,et al.  Corollary discharge across the animal kingdom , 2008, Nature Reviews Neuroscience.

[52]  K. Cullen.  Sensory signals during active versus passive movement , 2004, Current Opinion in Neurobiology.

[53]  Sofiane Cherif,et al.  An improved method for the estimation of firing rate dynamics using an optimal digital filter , 2008, Journal of Neuroscience Methods.

[54]  J. Goldberg,et al.  The vestibular nerve of the chinchilla. V. Relation between afferent discharge properties and peripheral innervation patterns in the utricular macula. , 1990, Journal of neurophysiology.

[55]  D. Angelaki,et al.  Spatial tuning and dynamics of vestibular semicircular canal afferents in rhesus monkeys , 2004, Experimental Brain Research.

[56]  R. Baker,et al.  Organization of the efferent, vestibular nuclei and nerves of the toadfish, Opsanus tau , 1986, The Journal of comparative neurology.

[57]  Kathleen E Cullen,et al.  Semicircular Canal Afferents Similarly Encode Active and Passive Head-On-Body Rotations: Implications for the Role of Vestibular Efference , 2002, The Journal of Neuroscience.

[58]  M. Correia,et al.  Bilateral communication between vestibular labyrinths in pigeons , 1993, Neuroscience.

[59]  F. Richmond,et al.  Control of head movement , 1988 .

[60]  Partha P. Mitra,et al.  Sampling Properties of the Spectrum and Coherency of Sequences of Action Potentials , 2000, Neural Computation.

[61]  Masao Ohmi,et al.  Heading judgments during active and passive self-motion , 2004, Experimental Brain Research.

[62]  M. Ohmi.  Egocentric perception through interaction among many sensory systems. , 1996, Brain research. Cognitive brain research.

[63]  M. Shinder,et al.  Vestibular efferent neurons project to the flocculus 1 1 Published on the World Wide Web on 6 December 2000. , 2001, Brain Research.

[64]  Ola Eiken,et al.  On the role of otoliths and semicircular canals in spatial orientation: Dynamics of the visually perceived eye level during gondola centrifugation , 2005, Perception & psychophysics.

[65]  H. Straka,et al.  Patterns of canal and otolith afferent input convergence in frog second-order vestibular neurons. , 2002, Journal of neurophysiology.

[66]  R. Llinás,et al.  The inhibitory vestibular efferent system and its relation to the cerebellum in the frog , 1969, Experimental Brain Research.

[67]  Theodore Raphan,et al.  Spatial properties of central vestibular neurons. , 2006, Journal of neurophysiology.

[68]  V. Han,et al.  Synaptic plasticity in the mormyrid electrosensory lobe. , 1999, The Journal of experimental biology.

[69]  R. J. Leigh,et al.  Frequency and velocity of rotational head perturbations during locomotion , 2004, Experimental Brain Research.

[70]  Daniel Guitton,et al.  The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics , 1996, Journal of Computational Neuroscience.

[71]  K. Cullen,et al.  Quantitative analysis of abducens neuron discharge dynamics during saccadic and slow eye movements. , 1999, Journal of neurophysiology.

[72]  M. Chacron,et al.  Neural Variability, Detection Thresholds, and Information Transmission in the Vestibular System , 2007, Journal of Neuroscience.

[73]  Dora E. Angelaki,et al.  Neurons compute internal models of the physical laws of motion , 2004, Nature.