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Passive rotation of the trunk with respect to the head evoked cervico-ocular reflex (COR) eye movements in squirrel monkeys. The amplitude of the reflex varied both within and between animals, but the eye movements were always in the same direction as trunk rotation. In the dark, the COR typically had a gain of 0.3-0.4. When animals fixated earth-stationary targets during low-frequency passive neck rotation or actively tracked moving visual targets with head movements, the COR was suppressed. The COR and vestibulo-ocular reflex (VOR) summed during passive head-on-trunk rotation producing compensatory eye movements whose gain was greater than 1.0. The firing behavior of VOR-related vestibular neurons and cerebellar flocculus Purkinje cells was studied during the COR. Passive neck rotation produced changes in firing rate related to neck position and/or neck velocity in both position-vestibular-pause neurons and eye-head-vestibular neurons, although the latter neurons were much more sensitive to the COR than the former. The neck rotation signals were reduced or reversed in direction when the COR was suppressed. Flocculus Purkinje cells were relatively insensitive to COR eye movements. However, when the COR was suppressed, their firing rate was modulated by neck rotation. These neck rotation signals summed with ocular pursuit signals when the head was used to pursue targets. We suggest that the neural substrate that produces the COR includes central VOR pathways, and that the flocculus plays an important role in suppressing the reflex when it would cause relative movement of a visual target on the retina.

The contribution of neck proprioceptive signals to signal processing in the vestibular nucleus was studied by recording responses of secondary horizontal canal-related neurons to neck rotation in the squirrel monkey. Responses evoked by passive neck rotation while the head was held stationary in space were compared with responses evoked by passive whole body rotation and by forced rotation of the head on the trunk. Most neurons (76%; 45/59) were sensitive to neck rotation. The nature and strength of neck proprioceptive inputs varied and usually combined linearly with vestibular inputs. In most cases (94%), the direction of the neck proprioceptive input was "antagonistic" or "reciprocal" with respect to vestibular sensitivity and, consequently, reduced the vestibular response during head-on-trunk rotation. Different types of vestibular neurons received different types of proprioceptive input. Neurons whose firing behavior was related to eye position (position-vestibular-pause neurons and position-vestibular neurons) were often sensitive to the position of the head with respect to the trunk. The sensitivity to head position was usually in the same direction as the neuron's eye position sensitivity. Non-eye-movement related neurons and eye-head-velocity neurons exhibited the strongest sensitivity to passive neck rotation and had signals that were best related to neck velocity. The results suggest that neck proprioceptive inputs play an important role in shaping the output of the primate vestibular nucleus and its contribution to posture, gaze and perception.

The contribution of irregular vestibular afferents to viewing distance-related changes in the angular vestibulo-ocular reflex (AVOR) and combined angular and linear VOR (CVOR) was studied in squirrel monkeys trained to fixate earth-stationary targets that were near (10 cm) and distant (90-170 cm) from their eyes. Perilymphatic anodal galvanic currents were used to reversibly silence irregular vestibular afferents for periods of 4-5 s during the AVOR and CVOR evoked by 0.5- to 4-Hz sinusoidal rotations (6-20 degrees/s peak velocity) or 250-400 degrees/s2 acceleration steps. The direction and magnitude of linear translation were changed by positioning the monkeys at different distances off the axis of turntable rotation. The effects of irregular afferent galvanic ablation (GA) on viewing distance-related changes in the AVOR were studied in four animals. Viewing distance-related changes in the AVOR could not always be evoked and were frequently small in amplitude. GA reduced viewing distance-related change in the AVOR by an average of 64% when it was present. Thus vestibular irregular afferents appear to play an important and necessary role in viewing distance-related changes in the AVOR - on those occasions when the changes occur. Viewing distance-related changes in the CVOR were large and reliably evoked. GA had very little effect on the gain or phase of viewing distance-related changes in the CVOR, although the viewing distance-related CVOR responses of individual central vestibular neurons were affected. We conclude that irregular afferents probably contribute to central signal processing related to both the AVOR and the CVOR, but the signals carried by these afferents are only essential for viewing distance-related changes in AVOR.

The discharge of neurons in the vestibular nuclei was recorded in alert squirrel monkeys while they were being sinusoidally rotated at 2 Hz. Type I position-vestibular-pause (PVP I) and vestibular-only (V I) neurons, as well as a smaller number of other type I and type II eye-plus-vestibular neurons were studied. Many of the neurons were monosynaptically related to the ipsilateral vestibular nerve. Eye-position and vestibular components of the rotation response were separated by multiple regression. Anodal currents, simultaneously delivered to both ears, were used to eliminate the head-rotation signals of irregularly discharging (I) vestibular-nerve afferents, presumably without affecting the corresponding signals of regularly discharging (R) afferents. R and I inputs to individual central neurons were determined by comparing rotation responses with and without the anodal currents. The bilateral currents, while reducing the background discharge of all types of neurons, did not affect the mean vestibular gain or phase calculated from a population of PVP I neurons or from a mixed population consisting of all type I units. From this result, it is concluded that I inputs are canceled at the level of secondary neurons. The cancellation may explain why the ablating currents do not affect the gain and phase of the vestibulo-ocular reflex. While cancellation was nearly perfect on a population basis, it was less so in individual neurons. For some neurons, the ablating currents decreased vestibular gain, while for other neurons the vestibular gain was increased. The former neurons are interpreted as receiving a net excitatory (I-EXC) I input, the latter neurons, a net inhibitory (I-INH) input. When compared with the corresponding R inputs, the I inputs were usually small and phase advanced. Phase advances were larger for I-EXC than for I-INH inputs. The sign and magnitude of the I inputs were unrelated to other discharge properties of individual neurons, including discharge regularity and the phase of vestibular responses measured in the absence of the ablating currents. Unilateral currents were used to assess the efficacy of ipsilateral and contralateral pathways. Ipsilateral pathways were responsible for almost all of the effects seen with bilateral currents. The results suggest that the vestibular signals carried by central neurons, even by those neurons receiving a monosynaptic vestibular-nerve input, are modified by polysynaptic pathways.

Squirrel monkeys were trained to cancel their vestibulo-ocular reflex (VOR) by fixating a visual target that was head stationary during passive vestibular stimulation. The monkeys were seated on a vestibular turntable, and their heads were restrained. A small visual target (0.2 degrees) was projected from the vestibular turntable onto a tangent screen. The monkeys' ability to suppress their VOR by fixating a head stationary target while the turntable was moving was compared to their ability to pursue the target when it was moved in the same manner. Squirrel monkeys were better able to suppress their VOR when the turntable was moved at high velocities than they were able to pursue targets that were moving at high velocities. The gaze velocity gain during VOR cancellation began to decrease when the head velocity was above 80 degrees/s, and was greater than 0.6 when the head velocity was above 150 degrees/s. However, gaze velocity gain during smooth pursuit decreased significantly when the target velocity was greater than 60 degrees/s, and was less than 0.4 when the target velocity was 150 degrees/s or more. The latency of VOR suppression was significantly shorter than the latency of smooth pursuit while the monkey was cancelling its VOR. When an unpredictable step change in head acceleration was generated while the monkey was cancelling its VOR, the VOR evoked by the head acceleration step began to be suppressed shortly after the initiation of the step (approximately 30 ms). On the other hand, the latency of the smooth pursuit eye movement elicited when the visual target was accelerated in the same manner during VOR cancellation was approximately 100 ms. The comparison between these two results suggests that the monkeys did not use visual information related to target motion to suppress their VOR at an early latency. The monkeys' ability to suppress the VOR evoked by an unexpected change in head acceleration depended on the size of the head acceleration step. The VOR evoked by unexpected step changes in head acceleration was progressively less suppressed at an early latency as the size of the acceleration step increased, and was not suppressed at an early latency when the step change in head acceleration was greater than 500 degrees/s2. During smooth pursuit eye movements, unexpected step changes in head acceleration evoked a VOR that was suppressed at an early latency (approximately 50 ms) if the head movement was in the same direction as the ongoing smooth pursuit eye movement.(ABSTRACT TRUNCATED AT 400 WORDS)

Recordings were made from secondary vestibular axons in the medial longitudinal fasciculus (MLF) of barbiturate-anesthetized squirrel monkeys. Antidromic stimulation techniques were used to identify the axons as belonging to one of three classes of neurons: vestibulo-oculo-collic (VOC) neurons project both to the extraocular motor nuclei and to the spinal cord; vestibulo-ocular (VO) neurons do not have a spinal projection; and vestibulocollic (VC) neurons do not have an oculo-motor projection. Galvanic stimulation was used to show that axons of all three classes received excitatory inputs from one labyrinth and inhibitory inputs from the other. VOC axons were confined to the MLF contralateral to the labyrinth from which they were excited. They made up more than half of the vestibular axons descending in the contralateral medial vestibulospinal tract (MVST), but less than one-quarter of those ascending in the contralateral MLF to the level of the oculomotor nucleus. Spinal projections were restricted to cervical segments with about half of the axons reaching segment C6. Conduction velocities, measured for C6-projecting axons, were similar for VOC and VC axons and were typically 25-50 m/s. Unlike the situation in the rabbit (Akaike et al. 1973) and cat (Akaike 1983), none of the MVST axons had conduction velocities greater than 75 m/s. The morphology of VOC neurons was studied by injection of horseradish peroxidase (HRP) into 60 physiologically identified axons in the MLF. Since individual axons were only stained for short distances, it was not possible to ascertain their complete branching patterns. Labeled fibers could be traced to an origin in and around the ventral lateral vestibular nucleus. This localization was confirmed by comparing the distributions within the vestibular nuclei of neurons retrogradely labeled from the upper cervical spinal cord (this study) and from the oculomotor nucleus (McCrea et al. 1987a; Highstein and McCrea 1988). VOC axons reached the contralateral MLF at the level of the abducens nucleus and immediately divided into an ascending and a descending, usually thicker, branch. Seven VOC axons could be traced to the extraocular motor nuclei; three terminated in the medial aspect of the oculomotor nucleus bilaterally and four terminated in the medial aspect of the contralateral abducens nucleus. The former axons may be part of a crossed, excitatory anterior-canal pathway; the latter, part of a similar horizontal-canal pathway. There were no terminations in the trochlear nucleus even though 12 labeled fibers passed close to it.(ABSTRACT TRUNCATED AT 400 WORDS)

Intracellular records were obtained from axons of second order vestibular neurons in, and around, the left abducens nucleus in alert cats implanted with stimulating electrodes on both vestibular nerves and the left VIth nerve. Twelve secondary vestibular neurons were identified by their increase in firing rate with horizontal head rotation to the left and/or increasing eye position to the right. Following HRP injection, somatic location, axonal trajectory and termination sites were determined. Each of the above cells collateralized extensively in the abducens nucleus in a fashion consistent with their being either inhibitory (n = 7; left) or excitatory (n = 6; right) vestibular neurons in the disynaptic horizontal vestibulo-ocular reflex pathway. These vestibular neurons also arborized extensively in other posterior brainstem eye-movement related areas as well as sending an axon to the spinal cord.

The morphology of secondary vertical vestibular neurons was investigated by injection of horseradish peroxidase (HRP) into cells connected to the posterior canal system in rabbits (lateral-eyed animals) and cats (frontal-eyed animals). Vestibular neurons were identified by stimulation with bipolar electrodes implanted into the ampullae of the anterior and posterior (PC) semicircular canals of pigmented rabbits; in the cat, these cells were identified by natural and electrical stimulation. Axons monosynaptically activated by PC stimulation were injected with HRP in the medial longitudinal fasciculus (MLF). These were later reconstructed by light microscopy after the brains had been processed with a DAB-CoCl2 method. In the rabbit the majority of the axons bifurcated after crossing the midline with one branch ascending and the other descending in the MLF. The ascending branches gave rise to collaterals that terminated in both the trochlear nucleus and the inferior rectus subdivision of the oculomotor nucleus. In addition some axons also sent collaterals into the paramedian pontine reticular formation, the periaqueductal grey and the interstitial nucleus of Cajal. The descending branches were followed to the caudal part of the medulla in the MLF and gave rise to collaterals terminating in the vestibular nuclei, the medullary reticular formation, the perihypoglossal nuclei, the abducens nucleus, and the facial nucleus. In another cell type axons crossed the midline without giving off any collaterals and proceeded caudally in the caudal MLF. The synaptic effects of the two types of cells were concluded to be excitatory and inhibitory, respectively. Cell bodies of contralaterally projecting neurons were located in either the medial or ventro-lateral vestibular nuclei. In the cat we observed two neuron classes, with contralaterally projecting axons, whose synaptic effects are presumably excitatory. Their cell somata were located in the medial vestibular nucleus. Termination patterns were similar to both the trochlear and oculomotor nuclei, but neither projected to the abducens nucleus. One class of neurons was almost identical to that found in the rabbit with the main axon bifurcating in the MLF. The second type lacked a descending branch in the MLF. Axon collaterals of the latter type crossed the midline within the oculomotor nucleus after terminating in the inferior rectus subdivision to reach a similar portion of the ipsilateral oculomotor nucleus. Collaterals of these axons also terminated bilaterally in the supraoculomotor region between trochlear and oculomotor nucleus, the interstitial nucleus of Cajal and prerubral loci (including the fields of Forel). In similarity to the rabbit, presumed inhibitory vestibular neurons were found with axons directed caudally in the MLF without brain stem collaterals.(ABSTRACT TRUNCATED AT 400 WORDS)

Saccadic omnipause neurons (OPNs) were intracellularly labelled with horseradish peroxidase (HRP) in alert cats and squirrel monkeys. The somas of OPNs were located on or near the midline in the caudal pons and their axons projected to regions of the pontomedullary reticular formation that contain the excitatory and inhibitory burst neurons.