Vestibular Perception in Time and Space During Whole-Body Rotation in Humans

Downbeat nystagmus (DBN) observed in head-hanging positions, may be of central or peripheral origin. Central DBN in head-hanging positions is mostly due to a disorder of the vestibulo-cerebellum, whereas peripheral DBN is usually attributed to canalolithiasis of an anterior semicircular canal. Here, we describe an atypical case of a patient who, after head trauma, experienced severe and stereotypic vertigo attacks after being placed in various head-hanging positions. Vertigo lasted 10–15 s and was always associated with a robust DBN. The provocation of transient vertigo and DBN, which both showed no decrease upon repetition of maneuvers, depended on the yaw orientation relative to the trunk and the angle of backward pitch. On a motorized, multi-axis turntable, we identified the two-dimensional Helmholtz coordinates of head positions at which vertigo and DBN occurred (y-axis: horizontal, space-fixed; z-axis: vertical, and head-fixed; x-axis: torsional, head-fixed, and unchanged). This two-dimensional area of DBN-associated head positions did not change when whole-body rotations took different paths (e.g., by forwarding pitch) or were executed with different velocities. Moreover, the intensity of DBN was also independent of whole-body rotation paths and velocities. So far, therapeutic approaches with repeated liberation maneuvers and cranial vibrations were not successful. We speculate that vertigo and DBN in this patient are due to macular damage, possibly an unstable otolithic membrane that, in specific orientations relative to gravity, slips into a position causing paroxysmal stimulation or inhibition of macular hair cells.

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Antihysteresis of perceived longitudinal body axis during continuous quasi-static whole-body rotation in the earth-vertical roll plane

Experimental Brain Research ◽

10.1007/s00221-011-2572-8 ◽

2011 ◽

Vol 209 (3) ◽

pp. 443-454

Author(s):

M. Tatalias ◽

C. J. Bockisch ◽

G. Bertolini ◽

D. Straumann ◽

A. Palla

Keyword(s):

Body Axis ◽

Whole Body ◽

Body Rotation ◽

Longitudinal Body Axis ◽

Vertical Roll ◽

The Earth

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Role of the Cerebellar Flocculus Region in the Coordination of Eye and Head Movements During Gaze Pursuit

Journal of Neurophysiology ◽

10.1152/jn.2000.84.3.1614 ◽

2000 ◽

Vol 84 (3) ◽

pp. 1614-1626 ◽

Cited By ~ 32

Author(s):

Timothy Belton ◽

Robert A. McCrea

Keyword(s):

Eye Movements ◽

Smooth Pursuit ◽

Head Movements ◽

Whole Body ◽

Head Tracking ◽

Smooth Pursuit Eye Movements ◽

Body Rotation ◽

Pursuit Eye Movements ◽

Smooth Tracking ◽

Eye Velocity

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive (≈43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.

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Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields (FEF) to whole body rotation

Neuroscience Research ◽

10.1016/j.neures.2007.06.1120 ◽

2007 ◽

Vol 58 ◽

pp. S95

Author(s):

Teppei Akao ◽

Hiroshi Saito ◽

Junko Fukushima ◽

Sergei Kurkin ◽

Kikuro Fukushima

Keyword(s):

Whole Body ◽

Frontal Eye Fields ◽

Body Rotation ◽

Pursuit Neurons

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Effects of listener’s whole-body rotation and sound duration on sound localization accuracy

The Journal of the Acoustical Society of America ◽

10.1121/1.5014754 ◽

2017 ◽

Vol 142 (4) ◽

pp. 2676-2676

Author(s):

Akio Honda ◽

Sayaka Tsunokake ◽

Yôiti Suzuki ◽

Shuichi Sakamoto

Keyword(s):

Sound Localization ◽

Whole Body ◽

Body Rotation ◽

Localization Accuracy ◽

Sound Duration

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Responses of Primate Caudal Parabrachial Nucleus and Kölliker-Fuse Nucleus Neurons to Whole Body Rotation

Journal of Neurophysiology ◽

10.1152/jn.00499.2002 ◽

2002 ◽

Vol 88 (6) ◽

pp. 3175-3193 ◽

Cited By ~ 27

Author(s):

Carey D. Balaban ◽

David M. McGee ◽

Jianxun Zhou ◽

Charles A. Scudder

Keyword(s):

Angular Velocity ◽

Vertical Plane ◽

Affective Responses ◽

Macaca Nemestrina ◽

Whole Body ◽

Vertical Position ◽

Limbic Cortex ◽

Body Rotation ◽

Spatial Tuning ◽

Position Sensitive

The caudal aspect of the parabrachial (PBN) and Kölliker-Fuse (KF) nuclei receive vestibular nuclear and visceral afferent information and are connected reciprocally with the spinal cord, hypothalamus, amygdala, and limbic cortex. Hence, they may be important sites of vestibulo-visceral integration, particularly for the development of affective responses to gravitoinertial challenges. Extracellular recordings were made from caudal PBN cells in three alert, adult female Macaca nemestrina through an implanted chamber. Sinusoidal and position trapezoid angular whole body rotation was delivered in yaw, roll, pitch, and vertical semicircular canal planes. Sites were confirmed histologically. Units that responded during rotation were located in lateral and medial PBN and KF caudal to the trochlear nerve at sites that were confirmed anatomically to receive superior vestibular nucleus afferents. Responses to whole-body angular rotation were modeled as a sum of three signals: angular velocity, a leaky integration of angular velocity, and vertical position. All neurons displayed angular velocity and integrated angular velocity sensitivity, but only 60% of the neurons were position-sensitive. These responses to vertical rotation could display symmetric, asymmetric, or fully rectified cosinusoidal spatial tuning about a best orientation in different cells. The spatial properties of velocity and integrated velocity and position responses were independent for all position-sensitive neurons; the angular velocity and integrated angular velocity signals showed independent spatial tuning in the position-insensitive neurons. Individual units showed one of three different orientations of their excitatory axis of velocity rotation sensitivity: vertical-plane-only responses, positive elevation responses (vertical plane plus ipsilateral yaw), and negative elevation axis responses (vertical plane plus negative yaw). The interactions between the velocity and integrated velocity components also produced variations in the temporal pattern of responses as a function of rotation direction. These findings are consistent with the hypothesis that a vestibulorecipient region of the PBN and KF integrates signals from the vestibular nuclei and relay information about changes in whole-body orientation to pathways that produce homeostatic and affective responses.

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Effects of listener's whole-body rotation and sound duration on horizontal sound localization accuracy

Acoustical Science and Technology ◽

10.1250/ast.39.305 ◽

2018 ◽

Vol 39 (4) ◽

pp. 305-307 ◽

Cited By ~ 2

Author(s):

Akio Honda ◽

Sayaka Tsunokake ◽

Yôiti Suzuki ◽

Shuichi Sakamoto

Keyword(s):

Sound Localization ◽

Whole Body ◽

Body Rotation ◽

Localization Accuracy ◽

Sound Duration

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Visual tracking with/without passive whole-body rotation in Parkinson’s disease (PD): Dissociation of smooth-pursuit and cancellation of vestibulo-ocular reflex (VOR)

Rinsho Shinkeigaku ◽

10.5692/clinicalneurol.cn-000766 ◽

2016 ◽

Vol 56 (3) ◽

pp. 158-164

Author(s):

Norie Ito ◽

Hidetoshi Takei ◽

Susumu Chiba ◽

Kiyoharu Inoue ◽

Kikuro Fukushima

Keyword(s):

Parkinson’S Disease ◽

Parkinson's Disease ◽

Visual Tracking ◽

Smooth Pursuit ◽

Whole Body ◽

Body Rotation ◽

Ocular Reflex ◽

Vestibulo Ocular Reflex

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Brain Stem Pursuit Pathways: Dissociating Visual, Vestibular, and Proprioceptive Inputs During Combined Eye-Head Gaze Tracking

Journal of Neurophysiology ◽

10.1152/jn.01074.2002 ◽

2003 ◽

Vol 90 (1) ◽

pp. 271-290 ◽

Cited By ~ 41

Author(s):

Jefferson E. Roy ◽

Kathleen E. Cullen

Keyword(s):

Smooth Pursuit ◽

Whole Body ◽

Eye Position ◽

Motor Nucleus ◽

Body Rotation ◽

Gaze Tracking ◽

Primary Input ◽

Passive Rotation ◽

Extraocular Motoneurons ◽

Movement Sensitivity

Eye-head (EH) neurons within the medial vestibular nuclei are thought to be the primary input to the extraocular motoneurons during smooth pursuit: they receive direct projections from the cerebellar flocculus/ventral paraflocculus, and in turn, project to the abducens motor nucleus. Here, we recorded from EH neurons during head-restrained smooth pursuit and head-unrestrained combined eye-head pursuit (gaze pursuit). During head-restrained smooth pursuit of sinusoidal and step-ramp target motion, each neuron's response was well described by a simple model that included resting discharge (bias), eye position, and velocity terms. Moreover, eye acceleration, as well as eye position, velocity, and acceleration error (error = target movement – eye movement) signals played no role in shaping neuronal discharges. During head-unrestrained gaze pursuit, EH neuron responses reflected the summation of their head-movement sensitivity during passive whole-body rotation in the dark and gaze-movement sensitivity during smooth pursuit. Indeed, EH neuron responses were well predicted by their head- and gaze-movement sensitivity during these two paradigms across conditions (e.g., combined eye-head gaze pursuit, smooth pursuit, whole-body rotation in the dark, whole-body rotation while viewing a target moving with the head (i.e., cancellation), and passive rotation of the head-on-body). Thus our results imply that vestibular inputs, but not the activation of neck proprioceptors, influence EH neuron responses during head-on-body movements. This latter proposal was confirmed by demonstrating a complete absence of modulation in the same neurons during passive rotation of the monkey's body beneath its neck. Taken together our results show that during gaze pursuit EH neurons carry vestibular- as well as gaze-related information to extraocular motoneurons. We propose that this vestibular-related modulation is offset by inputs from other premotor inputs, and that the responses of vestibuloocular reflex interneurons (i.e., position-vestibular-pause neurons) are consistent with such a proposal.

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