The integration of neural information by a passive kinetic stimulus and galvanic vestibular stimulation in the lateral vestibular nucleus

Despite an easy control and the direct effects on vestibular neurons, the clinical applications of galvanic vestibular stimulation (GVS) have been restricted because of its unclear activities as input. On the other hand, some critical conclusions have been made in the peripheral and the central processing of neural information by kinetic stimuli with different motion frequencies. Nevertheless, it is still elusive how the neural responses to simultaneous GVS and kinetic stimulus are modified during transmission and integration at the central vestibular area. To understand how the neural information was transmitted and integrated, we examined the neuronal responses to GVS, kinetic stimulus, and their combined stimulus in the vestibular nucleus. The neuronal response to each stimulus was recorded, and its responding features (amplitude and baseline) were extracted by applying the curve fitting based on a sinusoidal function. Twenty-five (96.2%) comparisons of the amplitudes showed that the amplitudes decreased during the combined stimulus (p < 0.001). However, the relations in the amplitudes (slope = 0.712) and the baselines (slope = 0.747) were linear. The neuronal effects by the different stimuli were separately estimated; the changes of the amplitudes were mainly caused by the kinetic stimulus and those of the baselines were largely influenced by GVS. Therefore, the slopes in the comparisons implied the neural sensitivity to the applied stimuli. Using the slopes, we found that the reduced amounts of the neural information were transmitted. Overall, the comparisons of the responding features demonstrated the linearity and the subadditivity in the neural transmission.

[1]  Andreas Zwergal,et al.  Vestibular animal models: contributions to understanding physiology and disease , 2016, Journal of Neurology.

[2]  B Bacchelli,et al.  The brain of the guinea pig in stereotaxic coordinates. , 1977, Archivio di scienze biologiche.

[3]  Mohsen Jamali,et al.  Integration of Canal and Otolith Inputs by Central Vestibular Neurons Is Subadditive for Both Active and Passive Self-Motion: Implication for Perception , 2015, The Journal of Neuroscience.

[4]  Colin Driscoll,et al.  Cervical VEMP threshold response curve in the identification of Ménière's disease. , 2014, Journal of the American Academy of Audiology.

[5]  F. E. Leon-Sarmiento,et al.  Galvanic vestibular stimulation: a novel modulatory countermeasure for vestibular-associated movement disorders. , 2014, Arquivos de neuro-psiquiatria.

[6]  M. Chacron,et al.  Information transmission and detection thresholds in the vestibular nuclei: single neurons vs. population encoding. , 2011, Journal of neurophysiology.

[7]  J. Dickman,et al.  Spatial and temporal characteristics of vestibular convergence , 2011, Neuroscience.

[8]  G. DeAngelis,et al.  Multisensory Integration in Macaque Visual Cortex Depends on Cue Reliability , 2008, Neuron.

[9]  M. Wallace,et al.  Representation and integration of multiple sensory inputs in primate superior colliculus. , 1996, Journal of neurophysiology.

[10]  Dora E Angelaki,et al.  Neural Correlates of Forward and Inverse Models for Eye Movements: Evidence from Three-Dimensional Kinematics , 2008, The Journal of Neuroscience.

[11]  Juno Kim,et al.  Responses of primary vestibular neurons to galvanic vestibular stimulation (GVS) in the anaesthetised guinea pig , 2004, Brain Research Bulletin.

[12]  Jaimie A. Roper,et al.  Deep brain stimulation improves gait velocity in Parkinson’s disease: a systematic review and meta-analysis , 2016, Journal of Neurology.

[13]  M. S. Cohen,et al.  Response of cat semicircular canal afferents to sinusoidal polarizing currents: implications for input-output properties of second-order neurons. , 1983, Journal of neurophysiology.

[14]  Md.Zakir Hossain Convergence patterns of the posterior semicircular canal and utricular inputs in single vestibular neurons in cats , 2001 .

[15]  Brian L Day,et al.  Probing the human vestibular system with galvanic stimulation. , 2004, Journal of applied physiology.

[16]  Sergei B. Yakushin,et al.  What Does Galvanic Vestibular Stimulation Actually Activate? , 2012, Front. Neur..

[17]  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.

[18]  E T Rolls,et al.  Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. , 1995, Journal of neurophysiology.

[19]  S. D. Lac,et al.  Frequency-Independent Synaptic Transmission Supports a Linear Vestibular Behavior , 2008, Neuron.

[20]  Kathleen E Cullen,et al.  Multisensory integration in early vestibular processing in mice: the encoding of passive vs. active motion. , 2013, Journal of neurophysiology.

[21]  D. R. Fish,et al.  Does electrical stimulation improve motor recovery in patients with idiopathic facial (Bell) palsy? , 2006, Physical Therapy.

[22]  W. King,et al.  Responses of monkey vestibular-only neurons to translation and angular rotation. , 2006, Journal of neurophysiology.

[23]  S. Lisberger Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. , 1994, Journal of neurophysiology.

[24]  T. Stanford,et al.  Evaluating the Operations Underlying Multisensory Integration in the Cat Superior Colliculus , 2005, The Journal of Neuroscience.

[25]  Jefferson E. Roy,et al.  Signal processing in the vestibular system during active versus passive head movements. , 2004, Journal of neurophysiology.

[26]  J. Goldberg Afferent diversity and the organization of central vestibular pathways , 2000, Experimental Brain Research.

[27]  Ian S. Curthoys,et al.  What Galvanic Vestibular Stimulation Actually Activates , 2012, Front. Neur..

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

[29]  Christophe Lopez,et al.  The vestibular system: balancing more than just the body. , 2016, Current opinion in neurology.

[30]  Adam D. Schneider,et al.  The Vestibular System Implements a Linear–Nonlinear Transformation In Order to Encode Self-Motion , 2012, PLoS biology.

[31]  B. Stein,et al.  Determinants of multisensory integration in superior colliculus neurons. I. Temporal factors , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  Richard C Fitzpatrick,et al.  What does galvanic vestibular stimulation stimulate? , 2002, Advances in experimental medicine and biology.

[33]  Lloyd B. Minor,et al.  Rotational Responses of Vestibular–Nerve Afferents Innervating the Semicircular Canals in the C57BL/6 Mouse , 2008, Journal of the Association for Research in Otolaryngology.

[34]  T. Murofushi,et al.  Clinical application of vestibular evoked myogenic potential (VEMP). , 2016, Auris, nasus, larynx.