Responses of Identified Vestibulospinal Neurons to Voluntary Eye and Head Movements in the Squirrel Monkey<sup>a</sup>

Boyle, R.; Belton, Timothy; McCrea, R. A.

doi:10.1111/j.1749-6632.1996.tb15704.x

Cited by 62 publications

(73 citation statements)

References 34 publications

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“…Neurons in the vestibular nucleus, which receive direct inputs from the vestibular afferents, are responsive to head velocity during passive whole-body rotations or passive head-on-body movements (Boyle et al, 1996;McCrea et al, 1999;Roy and Cullen, 2001). However, these same neurons do not provide reliable information during active movements of the head on the body.…”

Section: Discussionmentioning

confidence: 99%

“…Vestibular receptors and afferent fibers register information about the subject's own movement as well as movements that arise from changes in the external world (Cullen and Minor, 2002). However, a specific class of neurons in the vestibular nuclei, termed vestibular-only (VO) neurons, receive direct inputs from vestibular afferents but do not provide reliable information about head velocity during active rotations of the head on the body (Boyle et al, 1996;McCrea et al, 1999;Roy and Cullen, 2001). Remarkably, the same neurons continue to faithfully encode information about passive head rotations, which occur during the execution of voluntary movements.…”

Section: Introductionmentioning

confidence: 99%

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Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Roy¹,

Cullen²

2004

J. Neurosci.

217

177

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The ability to distinguish 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. To accomplish this, it has been proposed that an internal prediction of the consequences of our actions is compared with the actual sensory input to cancel the resultant self-generated activation. Here, we provide evidence for this hypothesis at an early stage of processing in the vestibular system. Previous studies have shown that neurons in the vestibular nucleus, which receive direct inputs from vestibular afferent fibers, are responsive to passively applied head movements. However, these same neurons do not reliably encode head velocity resulting from self-generated movements of the head on the body. In this study, we examined the mechanism that underlies the selective elimination of vestibular sensitivity to active head-on-body rotations. Individual neurons were recorded in monkeys making active head movements. The correspondence between intended and actual head movement was experimentally controlled. We found that a cancellation signal was gated into the vestibular nuclei only in conditions in which the activation of neckproprioceptorsmatchedthatexpectedonthebasisoftheneckmotorcommand.Thisfindingsuggeststhatvestibularsignalsthatarisefrom self-generated head movements are inhibited by a mechanism that compares the internal prediction of the sensory consequences by the brain to the actual resultant sensory feedback. Because self-generated vestibular inputs are selectively cancelled early in processing, we propose that this gating is important for the computation of spatial orientation and control of posture by higher-order structures.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Roy¹,

Cullen²

2004

J. Neurosci.

217

177

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“…In primates, each of the neuron classes supports different functions (reviewed in Cullen and Roy 2004). Although PVP and EH neurons generate the VOR and OKR via their direct projections to the extraocular motoneurons (Cullen and McCrea 1993;McCrea et al 1987;Roy and Cullen 2002;Scudder and Fuchs 1992), the descending projections of VO neurons to the spinal cord underlie postural reflexes such as the vestibulocollic reflex (Boyle 1993;Boyle et al 1996;Wilson et al 1990). Although recent studies have shown that this reflex is also robust in mouse (Baker 2005;Takemura and King 2005), whether the ES and VO neurons in mice subserve similar functions remains to be determined.…”

Section: Subpopulations Of Mouse Vn Neurons; Comparison With Other Spmentioning

confidence: 99%

Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse

Beraneck¹,

Cullen²

2007

Journal of Neurophysiology

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As a result of the availability of genetic mutant strains and development of noninvasive eye movements recording techniques, the mouse stands as a very interesting model for bridging the gap among behavioral responses, neuronal response dynamics studied in vivo, and cellular mechanisms investigated in vitro. Here we characterized the responses of individual neurons in the mouse vestibular nuclei during vestibular (horizontal whole body rotations) and full field visual stimulation. The majority of neurons (∼2/3) were sensitive to vestibular stimulation but not to eye movements. During the vestibular-ocular reflex (VOR), these neurons discharged in a manner comparable to the “vestibular only” (VO) neurons that have been previously described in primates. The remaining neurons [eye-movement-sensitive (ES) neurons] encoded both head-velocity and eye-position information during the VOR. When vestibular and visual stimulation were applied so that there was sensory conflict, the behavioral gain of the VOR was reduced. In turn, the modulation of sensitivity of VO neurons remained unaffected, whereas that of ES neurons was reduced. ES neurons were also modulated in response to full field visual stimulation that evoked the optokinetic reflex (OKR). Mouse VO neurons, however, unlike their primate counterpart, were not modulated during OKR. Taken together, our results show that the integration of visual and vestibular information in the mouse vestibular nucleus is limited to a subpopulation of neurons which likely supports gaze stabilization for both VOR and OKR.

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“…The VCR and CCR stabilize unexpected head movements with respect to space or with respect to the trunk (reviewed in , and there is evidence the signals carried by VCR pathways differ during active versus passive head movements (Boyle et al 1996;McCrea et al 1999;Cullen 2001, 2004). However, given that VCR and CCR gains are minimal in normal rhesus monkeys and humans (reviewed in Cullen and Roy 2004), it is unlikely that the differential modulation of these reflexes as a function of posture would play a primary role in altering the coordination of head and body movements.…”

Section: Influence Of Posture On the Coordination Of Eye-headbody Movmentioning

confidence: 99%

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

McCluskey

Cullen

2007

Journal of Neurophysiology

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McCluskey MK, Cullen KE. Eye, head, and body coordination during large gaze shifts in rhesus monkeys: movement kinematics and the influence of posture. J Neurophysiol 97: 2976 -2991, 2007. First published January 17, 2007 doi:10.1152/jn.00822.2006. Coordinated movements of the eye, head, and body are used to redirect the axis of gaze between objects of interest. However, previous studies of eyehead gaze shifts in head-unrestrained primates generally assumed the contribution of body movement to be negligible. Here we characterized eye-head-body coordination during horizontal gaze shifts made by trained rhesus monkeys to visual targets while they sat upright in a standard primate chair and assumed a more natural sitting posture in a custom-designed chair. In both postures, gaze shifts were characterized by the sequential onset of eye, head, and body movements, which could be described by predictable relationships. Body motion made a small but significant contribution to gaze shifts that were Ն40°i n amplitude. Furthermore, as gaze shift amplitude increased (40 -120°), body contribution and velocity increased systematically. In contrast, peak eye and head velocities plateaued at velocities of ϳ250 -300°/s, and the rotation of the eye-in-orbit and head-on-body remained well within the physical limits of ocular and neck motility during large gaze shifts, saturating at ϳ35 and 60°, respectively. Gaze shifts initiated with the eye more contralateral in the orbit were accompanied by smaller body as well as head movement amplitudes and velocities were greater when monkeys were seated in the more natural body posture. Taken together, our findings show that body movement makes a predictable contribution to gaze shifts that is systematically influenced by factors such as orbital position and posture. We conclude that body movements are part of a coordinated series of motor events that are used to voluntarily reorient gaze and that these movements can be significant even in a typical laboratory setting. Our results emphasize the need for caution in the interpretation of data from neurophysiological studies of the control of saccadic eye movements and/or eye-head gaze shifts because single neurons can code motor commands to move the body as well as the head and eyes.

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Responses of Identified Vestibulospinal Neurons to Voluntary Eye and Head Movements in the Squirrel Monkey^a

Cited by 62 publications

References 34 publications

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

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Responses of Identified Vestibulospinal Neurons to Voluntary Eye and Head Movements in the Squirrel Monkeya

Cited by 62 publications

References 34 publications

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Dissociating Self-Generated from Passively Applied Head Motion: Neural Mechanisms in the Vestibular Nuclei

Activity of Vestibular Nuclei Neurons During Vestibular and Optokinetic Stimulation in the Alert Mouse

Eye, Head, and Body Coordination During Large Gaze Shifts in Rhesus Monkeys: Movement Kinematics and the Influence of Posture

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Product

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Responses of Identified Vestibulospinal Neurons to Voluntary Eye and Head Movements in the Squirrel Monkey^a