Vestibular response kinematics in posterior parietal cortex neurons of macaque monkeys

Perception of extrapersonal space is a fundamental requirement for accurate interaction with the environment and moving in it. Parietal cortical areas are thought to play an important role in this function. A significant sensory input to this area arrives from the vestibular system. We quantified neuronal responses in the ventral intraparietal area and the medial intraparietal area of awake head‐fixed macaque monkeys during classical vestibular sinusoidal stimulation protocols and with a newly developed random vestibular testing paradigm. The goal was to study more specifically the signal content of perietal vestibular neurons with respect to head movement kinematics. Traditional sinusoidal stimulation analysis revealed that about one‐third of the neurons responded in phase with either head position or head acceleration, besides classical head velocity tuning. Random vestibular stimulation revealed more complex signal profiles in the majority of neurons, although quantification of the kinematic variables that drove the neurons most effectively led to similar results to phase shift analysis. Thus, a majority of cells was principally driven by head velocity, and a minority by either acceleration or position. Nevertheless, random stimulation also revealed the simultaneous presence of all three kinematic response parameters (i.e. velocity, position and acceleration) in a majority of neurons. A minority of cells coded only two kinematic variables, i.e. head velocity coupled with either acceleration or position. Neurons coding only one kinematic variable were not found. We hereby demonstrate for the first time that central vestibular neurons carry several head movement kinematic variables simultaneously.

[1]  J. Taube,et al.  Processing the head direction cell signal: A review and commentary , 1996, Brain Research Bulletin.

[2]  F. Bremmer,et al.  Spatial invariance of visual receptive fields in parietal cortex neurons , 1997, Nature.

[3]  C. L. Mallows Some comments on C_p , 1973 .

[4]  E. Rolls,et al.  Head direction cells in the primate pre‐subiculum , 1999, Hippocampus.

[5]  D. V. van Essen,et al.  Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey , 2000, The Journal of comparative neurology.

[6]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. I. A continuum of response selectivity to large-field stimuli. , 1991, Journal of neurophysiology.

[7]  K. Schaefer,et al.  Die Neuronenaktivität in der Formatio reticularis des Rhombencephalons beim vestibulären Nystagmus , 2005, Archiv für Psychiatrie und Nervenkrankheiten.

[8]  O. Grüsser,et al.  Responses of Single Neurons in the Parietoinsular Vestibular Cortex of Primates a , 1988, Annals of the New York Academy of Sciences.

[9]  R. Wurtz,et al.  Sensitivity of MST neurons to optic flow stimuli. II. Mechanisms of response selectivity revealed by small-field stimuli. , 1991, Journal of neurophysiology.

[10]  R H Schor,et al.  Responses to head tilt in cat central vestibular neurons. I. Direction of maximum sensitivity. , 1984, Journal of neurophysiology.

[11]  John H. R. Maunsell,et al.  The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  A. Rubens Caloric stimulation and unilateral visual neglect , 1985, Neurology.

[13]  R. Andersen Encoding of intention and spatial location in the posterior parietal cortex. , 1995, Cerebral cortex.

[14]  C. Mallows More comments on C p , 1995 .

[15]  Michael G. Paulin Digital filters for firing rate estimation , 2004, Biological Cybernetics.

[16]  Jacques Droulez,et al.  Does the brain use sliding variables for the control of movements? , 1997, Biological Cybernetics.

[17]  S. Ben Hamed,et al.  Representation of the visual field in the lateral intraparietal area of macaque monkeys: a quantitative receptive field analysis , 2001, Experimental Brain Research.

[18]  J. Assad,et al.  Dissociation of visual, motor and predictive signals in parietal cortex during visual guidance , 1999, Nature Neuroscience.

[19]  J. Taube,et al.  Hippocampal spatial representations require vestibular input , 2002, Hippocampus.

[20]  R. Andersen,et al.  Head position signals used by parietal neurons to encode locations of visual stimuli , 1995, Nature.

[21]  J R Duhamel,et al.  The updating of the representation of visual space in parietal cortex by intended eye movements. , 1992, Science.

[22]  Frank Bremmer,et al.  ã Federation of European Neuroscience Societies Heading encoding in the macaque ventral intraparietal area (VIP) , 2022 .

[23]  Richard A. Andersen,et al.  Separate body- and world-referenced representations of visual space in parietal cortex , 1998, Nature.

[24]  J. M. Fredrickson,et al.  Projection of the vestibular nerve to the area 3a arm field in the squirrel monkey (Saimiri Sciureus) , 2004, Experimental Brain Research.

[25]  V. Mountcastle,et al.  Posterior parietal association cortex of the monkey: command functions for operations within extrapersonal space. , 1975, Journal of neurophysiology.

[26]  U. W. Buettner,et al.  Parietal cortex (2v) neuronal activity in the alert monkey during natural vestibular and optokinetic stimulation , 1978, Brain Research.

[27]  R. Andersen,et al.  The Contributions of Vestibular Signals to the Representations of Space in the Posterior Parietal Cortex , 1999, Annals of the New York Academy of Sciences.

[28]  David N. Lee 16 Visuo-Motor Coordination in Space-Time , 1980 .

[29]  R. Andersen,et al.  Electrical microstimulation distinguishes distinct saccade-related areas in the posterior parietal cortex. , 1998, Journal of neurophysiology.

[30]  R. M. Siegel,et al.  Encoding of spatial location by posterior parietal neurons. , 1985, Science.

[31]  Edoardo Bisiach,et al.  The Spatial Features of Unilateral Neglect , 1997 .

[32]  J. Hopfield,et al.  Electrical microstimulation suggests two different forms of representation of head-centered space in the intraparietal sulcus of rhesus monkeys. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[33]  M. Critchleey [Parietal lobes]. , 1953, Giornale di psichiatria e di neuropatologia.

[34]  O. Grüsser,et al.  Cortico‐cortical connections and cytoarchitectonics of the primate vestibular cortex: A study in squirrel monkeys (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[35]  D. V. van Essen,et al.  Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto‐occipital cortex , 2000, The Journal of comparative neurology.

[36]  A. Toga,et al.  The Rhesus Monkey Brain in Stereotaxic Coordinates , 1999 .

[37]  L. Swan,et al.  Unilateral spatial neglect. , 2001, Physical therapy.

[38]  J. Taube,et al.  Firing Properties of Head Direction Cells in the Rat Anterior Thalamic Nucleus: Dependence on Vestibular Input , 1997, The Journal of Neuroscience.

[39]  Hideo Sakata,et al.  Functional properties of rotation-sensitive neurons in the posterior parietal association cortex of the monkey , 1994, Experimental Brain Research.

[40]  N. Draper,et al.  Applied Regression Analysis: Draper/Applied Regression Analysis , 1998 .

[41]  F Bremmer,et al.  Eye position encoding in the macaque ventral intraparietal area (VIP). , 1999, Neuroreport.

[42]  Adonis Moschovakis,et al.  Density gradients of trans‐synaptically labeled collicular neurons after injections of rabies virus in the lateral rectus muscle of the rhesus monkey , 2002, The Journal of comparative neurology.

[43]  François Klam,et al.  ã Federation of European Neuroscience Societies Visual±vestibular interactive responses in the macaque ventral intraparietal area (VIP) , 2022 .

[44]  C. Colby,et al.  Heterogeneity of extrastriate visual areas and multiple parietal areas in the Macaque monkey , 1991, Neuropsychologia.

[45]  Frank Bremmer,et al.  The Representation of Movement in Near Extra-Personal Space in the Macaque Ventral Intraparietal Area (VIP) , 1997 .

[46]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

[47]  D. Schwarz,et al.  Rhesus Monkey Vestibular Cortex: A Bimodal Primary Projection Field , 1971, Science.

[48]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: anatomic location and visual response properties. , 1993, Journal of neurophysiology.

[49]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[50]  M. Goldberg,et al.  Ventral intraparietal area of the macaque: congruent visual and somatic response properties. , 1998, Journal of neurophysiology.

[51]  Werner Graf,et al.  Mapping the oculomotor system: the power of transneuronal labelling with rabies virus , 2002, The European journal of neuroscience.