Firing Behavior of Vestibular Neurons During Active and Passive Head Movements: Vestibulo-Spinal and Other Non-Eye-Movement Related Neurons

1999 ◽  
Vol 82 (1) ◽  
pp. 416-428 ◽  
Author(s):  
Robert A. McCrea ◽  
Greg T. Gdowski ◽  
Richard Boyle ◽  
Timothy Belton
Keyword(s):  
Electrical Stimulation ◽  
Eye Movement ◽  
Head Rotation ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Firing Behavior ◽  
Vestibular Neurons ◽  
Gaze Saccades ◽  
Stimulation Of

The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units ( n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20–75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.

Integration of Vestibular and Head Movement Signals in the Vestibular Nuclei During Whole-Body Rotation

1999 ◽  
Vol 82 (1) ◽  
pp. 436-449 ◽  
Author(s):  
Greg T. Gdowski ◽  
Robert A. McCrea
Keyword(s):  
Eye Movement ◽  
Head Rotation ◽  
Vestibular Nuclei ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Horizontal Semicircular Canal ◽  
Head Velocity ◽  
Vestibular Neurons ◽  
Single Unit Recordings

Single-unit recordings were obtained from 107 horizontal semicircular canal-related central vestibular neurons in three alert squirrel monkeys during passive sinusoidal whole-body rotation (WBR) while the head was free to move in the yaw plane (2.3 Hz, 20°/s). Most of the units were identified as secondary vestibular neurons by electrical stimulation of the ipsilateral vestibular nerve (61/80 tested). Both non–eye-movement ( n = 52) and eye-movement–related ( n = 55) units were studied. Unit responses recorded when the head was free to move were compared with responses recorded when the head was restrained from moving. WBR in the absence of a visual target evoked a compensatory vestibulocollic reflex (VCR) that effectively reduced the head velocity in space by an average of 33 ± 14%. In 73 units, the compensatory head movements were sufficiently large to permit the effect of the VCR on vestibular signal processing to be assessed quantitatively. The VCR affected the rotational responses of different vestibular neurons in different ways. Approximately one-half of the units (34/73, 47%) had responses that decreased as head velocity decreased. However, the responses of many other units (24/73) showed little change. These cells had signals that were better correlated with trunk velocity than with head velocity. The remaining units had responses that were significantly larger (15/73, 21%) when the VCR produced a decrease in head velocity. Eye-movement–related units tended to have rotational responses that were correlated with head velocity. On the other hand, non–eye-movement units tended to have rotational responses that were better correlated with trunk velocity. We conclude that sensory vestibular signals are transformed from head-in-space coordinates to trunk-in-space coordinates on many secondary vestibular neurons in the vestibular nuclei by the addition of inputs related to head rotation on the trunk. This coordinate transformation is presumably important for controlling postural reflexes and constructing a central percept of body orientation and movement in space.

Vestibuloocular Reflex Signal Modulation During Voluntary and Passive Head Movements

2002 ◽  
Vol 87 (5) ◽  
pp. 2337-2357 ◽  
Author(s):  
Jefferson E. Roy ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movement ◽  
Head Movements ◽  
Body Motion ◽  
Whole Body ◽  
Type I ◽  
Vestibuloocular Reflex ◽  
Body Rotation ◽  
Gaze Shifts ◽  
Head Velocity ◽  
Wide Range

The vestibuloocular reflex (VOR) effectively stabilizes the visual world on the retina over the wide range of head movements generated during daily activities by producing an eye movement of equal and opposite amplitude to the motion of the head. Although an intact VOR is essential for stabilizing gaze during walking and running, it can be counterproductive during certain voluntary behaviors. For example, primates use rapid coordinated movements of the eyes and head (gaze shifts) to redirect the visual axis from one target of interest to another. During these self-generated head movements, a fully functional VOR would generate an eye-movement command in the direction opposite to that of the intended shift in gaze. Here, we have investigated how the VOR pathways process vestibular information across a wide range of behaviors in which head movements were either externally applied and/or self-generated and in which the gaze goal was systematically varied (i.e., stabilize vs. redirect). VOR interneurons [i.e., type I position-vestibular-pause (PVP) neurons] were characterized during head-restrained passive whole-body rotation, passive head-on-body rotation, active eye-head gaze shifts, active eye-head gaze pursuit, self-generated whole-body motion, and active head-on-body motion made while the monkey was passively rotated. We found that regardless of the stimulation condition, type I PVP neuron responses to head motion were comparable whenever the monkey stabilized its gaze. In contrast, whenever the monkey redirected its gaze, type I PVP neurons were significantly less responsive to head velocity. We also performed a comparable analysis of type II PVP neurons, which are likely to contribute indirectly to the VOR, and found that they generally behaved in a quantitatively similar manner. Thus our findings support the hypothesis that the activity of the VOR pathways is reduced “on-line” whenever the current behavioral goal is to redirect gaze. By characterizing neuronal responses during a variety of experimental conditions, we were also able to determine which inputs contribute to the differential processing of head-velocity information by PVP neurons. We show that neither neck proprioceptive inputs, an efference copy of neck motor commands nor the monkey's knowledge of its self-motion influence the activity of PVP neurons per se. Rather we propose that efference copies of oculomotor/gaze commands are responsible for the behaviorally dependent modulation of PVP neurons (and by extension for modulation of the status of the VOR) during gaze redirection.

scholarly journals Galvanic stimulation of the vestibular periphery in guinea pigs during passive whole body rotation and self-generated head movement

2012 ◽  
Vol 107 (8) ◽  
pp. 2260-2270 ◽  
Author(s):  
N. Shanidze ◽  
K. Lim ◽  
J. Dye ◽  
W. M. King
Keyword(s):  
Guinea Pigs ◽  
Head Movements ◽  
Whole Body ◽  
Body Rotation ◽  
Galvanic Stimulation ◽  
Ocular Reflex ◽  
Anticipatory Eye Movements ◽  
Vestibulo Ocular Reflex ◽  
Vestibulospinal Neurons ◽  
Stimulation Of

Irregular vestibular afferents exhibit significant phase leads with respect to angular velocity of the head in space. This characteristic and their connectivity with vestibulospinal neurons suggest a functionally important role for these afferents in producing the vestibulo-collic reflex (VCR). A goal of these experiments was to test this hypothesis with the use of weak galvanic stimulation of the vestibular periphery (GVS) to selectively activate or suppress irregular afferents during passive whole body rotation of guinea pigs that could freely move their heads. Both inhibitory and excitatory GVS had significant effects on compensatory head movements during sinusoidal and transient whole body rotations. Unexpectedly, GVS also strongly affected the vestibulo-ocular reflex (VOR) during passive whole body rotation. The effect of GVS on the VOR was comparable in light and darkness and whether the head was restrained or unrestrained. Significantly, there was no effect of GVS on compensatory eye and head movements during volitional head motion, a confirmation of our previous study that demonstrated the extravestibular nature of anticipatory eye movements that compensate for voluntary head movements.

Effects of Viewing Distance on the Responses of Horizontal Canal–Related Secondary Vestibular Neurons During Angular Head Rotation

1999 ◽  
Vol 81 (5) ◽  
pp. 2517-2537 ◽  
Author(s):  
Chiju Chen-Huang ◽  
Robert A. McCrea
Keyword(s):  
Eye Movements ◽  
Eye Movement ◽  
Head Rotation ◽  
Vestibular Nerve ◽  
Viewing Distance ◽  
Vestibuloocular Reflex ◽  
Horizontal Canal ◽  
Head Velocity ◽  
Firing Behavior ◽  
Vestibular Neurons

Effects of viewing distance on the responses of horizontal canal–related secondary vestibular neurons during angular head rotation. The eye movements generated by the horizontal canal–related angular vestibuloocular reflex (AVOR) depend on the distance of the image from the head and the axis of head rotation. The effects of viewing distance on the responses of 105 horizontal canal–related central vestibular neurons were examined in two squirrel monkeys that were trained to fixate small, earth-stationary targets at different distances (10 and 150 cm) from their eyes. The majority of these cells (77/105) were identified as secondary vestibular neurons by synaptic activation following electrical stimulation of the vestibular nerve. All of the viewing distance–sensitive units were also sensitive to eye movements in the absence of head movements. Some classes of eye movement–related vestibular units were more sensitive to viewing distance than others. For example, the average increase in rotational gain (discharge rate/head velocity) of position-vestibular-pause units was 20%, whereas the gain increase of eye-head-velocity units was 44%. The concomitant change in gain of the AVOR was 11%. Near viewing responses of units phase lagged the responses they generated during far target viewing by 6–25°. A similar phase lag was not observed in either the near AVOR eye movements or in the firing behavior of burst-position units in the vestibular nuclei whose firing behavior was only related to eye movements. The viewing distance–related increase in the evoked eye movements and in the rotational gain of all unit classes declined progressively as stimulus frequency increased from 0.7 to 4.0 Hz. When monkeys canceled their VOR by fixating head-stationary targets, the responses recorded during near and far target viewing were comparable. However, the viewing distance–related response changes exhibited by central units were not directly attributable to the eye movement signals they generated. Subtraction of static eye position signals reduced, but did not abolish viewing distance gain changes in most units. Smooth pursuit eye velocity sensitivity and viewing distance sensitivity were not well correlated. We conclude that the central premotor pathways that mediate the AVOR also mediate viewing distance–related changes in the reflex. Because irregular vestibular nerve afferents are necessary for viewing distance–related gain changes in the AVOR, we suggest that a central estimate of viewing distance is used to parametrically modify vestibular afferent inputs to secondary vestibuloocular reflex pathways.

scholarly journals Electrical Stimulation of the Frontal Eye Field in a Monkey Produces Combined Eye and Head Movements

2000 ◽  
Vol 84 (2) ◽  
pp. 1103-1106 ◽  
Author(s):  
Tyson A. Tu ◽  
E. Gregory Keating
Keyword(s):  
Electrical Stimulation ◽  
Eye Movements ◽  
Head Movements ◽  
Frontal Eye Field ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
Eye Field ◽  
A Site ◽  
Head Rotations ◽  
Stimulation Of

The frontal eye field (FEF), an area in the primate frontal lobe, has long been considered important for the production of eye movements. Past studies have evoked saccade-like movements from the FEF using electrical stimulation in animals that were not allowed to move their heads. Using electrical stimulation in two monkeys that were free to move their heads, we have found that the FEF produces gaze shifts that are composed of both eye and head movements. Repeated stimulation at a site evoked gaze shifts of roughly constant amplitude. However, that gaze shift could be accomplished with varied amounts of head and eye movements, depending on their (head and eye) respective starting positions. This evidence suggests that the FEF controls visually orienting movements using both eye and head rotations rather than just shifting the eyes as previously thought.

Effect of Adaptation to Telescopic Spectacles on the Initial Human Horizontal Vestibuloocular Reflex

2000 ◽  
Vol 83 (1) ◽  
pp. 38-49 ◽  
Author(s):  
Benjamin T. Crane ◽  
Joseph L. Demer
Keyword(s):  
Head Rotation ◽  
Head Movements ◽  
Target Distance ◽  
Whole Body ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Head Acceleration ◽  
Gain Enhancement ◽  
Lower Head ◽  
Distant Target

Gain of the vestibuloocular reflex (VOR) not only varies with target distance and rotational axis, but can be chronically modified in response to prolonged wearing of head-mounted magnifiers. This study examined the effect of adaptation to telescopic spectacles on the variation of the VOR with changes in target distance and yaw rotational axis for head velocity transients having peak accelerations of 2,800 and 1,000°/s2. Eye and head movements were recorded with search coils in 10 subjects who underwent whole body rotations around vertical axes that were 10 cm anterior to the eyes, centered between the eyes, between the otoliths, or 20 cm posterior to the eyes. Immediately before each rotation, subjects viewed a target 15 or 500 cm distant. Lighting was extinguished immediately before and was restored after completion of each rotation. After initial rotations, subjects wore 1.9× magnification binocular telescopic spectacles during their daily activities for at least 6 h. Test spectacles were removed and measurement rotations were repeated. Of the eight subjects tolerant of adaptation to the telescopes, six demonstrated VOR gain enhancement after adaptation, while gain in two subjects was not increased. For all subjects, the earliest VOR began 7–10 ms after onset of head rotation regardless of axis eccentricity or target distance. Regardless of adaptation, VOR gain for the proximate target exceeded that for the distant target beginning at 20 ms after onset of head rotation. Adaptation increased VOR gain as measured 90–100 ms after head rotation onset by an average of 0.12 ± 0.02 (SE) for the higher head acceleration and 0.19 ± 0.02 for the lower head acceleration. After adaptation, four subjects exhibited significant increases in the canal VOR gain only, whereas two subjects exhibited significant increases in both angular and linear VOR gains. The latencies of linear and early angular target distance effects on VOR gain were unaffected by adaptation. The earliest significant change in angular VOR gain in response to adaptation occurred 50 and 68 ms after onset of the 2,800 and 1,000°/s2 peak head accelerations, respectively. The latency of the adaptive increase in linear VOR gain was ∼50 ms for the peak head acceleration of 2,800°/s2, and 100 ms for the peak head acceleration of 1,000°/s2. Thus VOR gain changes and latency were consistent with modification in the angular VOR in most subjects, and additionally in the linear VOR in a minority of subjects.

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

2000 ◽  
Vol 84 (3) ◽  
pp. 1614-1626 ◽  
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.

scholarly journals Canal-Specific Excitation and Inhibition of Frog Second-Order Vestibular Neurons

1997 ◽  
Vol 78 (3) ◽  
pp. 1363-1372 ◽  
Author(s):  
H. Straka ◽  
S. Biesdorf ◽  
N. Dieringer
Keyword(s):  
Electrical Stimulation ◽  
Semicircular Canal ◽  
Second Order ◽  
Projection Neurons ◽  
Postsynaptic Potentials ◽  
Vestibular Neurons ◽  
Inhibitory Postsynaptic Potentials ◽  
Monosynaptic Epsp ◽  
Stimulation Of ◽  
Monosynaptic Excitation

Straka, H., S. Biesdorf, and N. Dieringer. Canal-specific excitation and inhibition of frog second-order vestibular neurons. J. Neurophysiol. 78: 1363–1372, 1997. Second-order vestibular neurons (2°VNs) were identified in the in vitro frog brain by their monosynaptic excitation following electrical stimulation of the ipsilateral VIIIth nerve. Ipsilateral disynaptic inhibitory postsynaptic potentials were revealed by bath application of the glycine antagonist strychnine or of the γ-aminobutyric acid-A (GABAA) antagonist bicuculline. Ipsilateral disynaptic excitatory postsynaptic potentials (EPSPs) were analyzed as well. The functional organization of convergent monosynaptic and disynaptic excitatory and inhibitory inputs onto 2°VNs was studied by separate electrical stimulation of individual semicircular canal nerves on the ipsilateral side. Most 2°VNs (88%) received a monosynaptic EPSP exclusively from one of the three semicircular canal nerves; fewer 2°VNs (10%) were monosynaptically excited from two semicircular canal nerves; and even fewer 2°VNs (2%) were monosynaptically excited from each of the three semicircular canal nerves. Disynaptic EPSPs were present in the majority of 2°VNs (68%) and originated from the same (homonymous) semicircular canal nerve that activated a monosynaptic EPSP in a given neuron (22%), from one or both of the other two (heteronymous) canal nerves (18%), or from all three canal nerves (28%). Homonymous activation of disynaptic EPSPs prevailed (74%) among those 2°VNs that exhibited disynaptic EPSPs. Disynaptic inhibitory postsynaptic potentials (IPSPs) were mediated in 90% of the tested 2°VNs by glycine, in 76% by GABA, and in 62% by GABA as well as by glycine. These IPSPs were activated almost exclusively from the same semicircular canal nerve that evoked the monosynaptic EPSP in a given 2°VN. Our results demonstrate a canal-specific, modular organization of vestibular nerve afferent fiber inputs onto 2°VNs that consists of a monosynaptic excitation from one semicircular canal nerve followed by disynaptic excitatory and inhibitory inputs originating from the homonymous canal nerve. Excitatory and inhibitory second-order (2°) vestibular interneurons are envisaged to form side loops that mediate spatially similar but dynamically different signals to 2° vestibular projection neurons. These feedforward side loops are suited to adjust the dynamic response properties of 2° vestibular projection neurons by facilitating or disfacilitating phasic and tonic input components.

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