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Translational motion induces retinal image slip which varies with object distance. The brain must know binocular eye position in real time in order to scale eye movements so as to minimize retinal slip. Two potential sources of eye position information are orbital proprioception and an internal representation of eye position derived from central ocular motor signals. To examine the role of orbital proprioceptive information, the position of the left eye was perturbed by microstimulation of the left abducens nerve during translational motion to the right or left along the interaural axis in two rhesus macaques. Microstimulation rotated the eye laterally, activating eye muscle proprioceptors, while keeping central motor commands undisturbed. We found that microstimulation-induced eye position changes did not affect the translational VOR in the abductive (lateral rectus) direction, but it did influence the responses in the adductive (medial rectus) direction. Our findings demonstrate that proprioceptive inputs appear to be involved in the TVOR responses at least during ipsilateral head movements and proprioceptive influences on the TVOR may involve vergence-related signals to the oculomotor nucleus. However, internal representation of eye position, derived from central ocular motor signals, likely plays the dominant role in providing eye position information for scaling eye movements during translational motion, particularly in the abducent direction.

In the present study, we report the sensitivity of utricular afferents to sinusoidal translational motion in the horizontal plane. The head orientation was altered relative to the direction of translational travel in 30 degrees increments to allow determination of the head orientation that elicited the maximal and minimal responses of each afferent neuron. We determined gain and phase relationships at a constant peak linear acceleration of 0.1 g applied at frequencies between 0.20 and 2.0 Hz for multiple head orientations. The response dynamics and vector of maximal sensitivity for the utricular afferents are consistent with those reported for other mammalian species. Irregularly (CV>0.3) and intermediate (0.1

Following the orienting saccade of a combined eye-head gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) of near unity, is a manifestation of the vestibulo-ocular reflex (VOR). Acute unilateral labyrinthectomy (UL) causes severe asymmetry in the VOR during passive head rotations that recovers incompletely over time. The purpose of this investigation was to compare the recovery of the counterrotation gain during horizontal gaze shifts with that of the passive VOR after UL. During the 1st week after UL, counterrotation gains were asymmetric, being lower for head movements towards the lesion but nearly normal for head movements towards the intact side. Whereas this asymmetry in the counterrotation gain resolved within a week after UL, asymmetries in the passive VOR persisted. During the 1st week after UL, behavioral performance was generally poor, with a high incidence of inaccurate gaze shifts and larger latencies. In addition, animals used slower head movements such that peak head amplitude during the eye saccade was significantly lower during the 1st week after UL as compared to control values. Bilateral labyrinthectomy (BL) resulted in larger but symmetric deficits in counterrotation, which, contrary to the passive VOR, exhibited significant recovery over time. It is hypothesized that recovery of counterrotation gain after UL has contributions from multiple sources, including the contralateral intact labyrinth and an efference copy of the head movement.

The spontaneous activity and dynamic responses to two frequencies (1.3 and 0.13 Hz) of sinusoidal angular horizontal head acceleration of type I neurons in the medial vestibular nucleus were recorded bilaterally in decerebrate Mongolian gerbils (Meriones unguiculatus) under three experimental conditions; normal labyrinth intact, acutely following unilateral labyrinthine lesion, and four to seven weeks following labyrinthine lesion. The mean spontaneous activity and number of detected type I neurons decreased immediately ipsilateral to the lesion but recovered significantly with time. In contrast, spontaneous activity on the contralateral side increased during compensation following hemilabyrinthectomy. The mean response gains at both frequencies of head oscillation were depressed bilaterally and asymmetrically acutely following the lesion such that the response gain of cells on the intact side exceeded that of the neurons recorded on the injured side. After compensation the number of detected type I neurons on the side ipsilateral to the injury increased but remained below normal levels. The mean gains remained depressed but became symmetric with compensation as a result of improvement in the response of ipsilateral neurons. The phase of responses were significantly advanced in the compensated animals. Although response gain is not fully restored, the linearity of the dynamic modulation in compensated animals is improved as evidenced by a continuous modulation of the increased spontaneous activity of neurons contralateral to the hemilabyrinthectomy. It is proposed that this effect is related to the concurrent improvement in the linearity of the horizontal vestibulo-ocular response. Electrical cathodal polarization of the vestibular nerve ipsilateral to the ablated labyrinth was utilized to investigate the relationship between recovery of spontaneous activity and dynamic function. Acutely following hemilabyrinthectomy, cathodal polarization restored activity in second-order type I neurons to near normal levels but their response gain to head rotation remained depressed. Similar galvanic stimulation in compensated animals also elevated ipsilateral spontaneous activity. As in the acute preparation, such stimulation did not modify the response gain or phase. Thus, the improvement in response of type I neurons in the compensated gerbil was not a direct consequence of restoration of spontaneous activity on the side of the injury.

The spontaneous activity and dynamic responses to sinusoidal horizontal head angular acceleration of type II horizontal semicircular canal related neurons in the medial vestibular nucleus (MVN) were recorded bilaterally in decerebrate Mongolian gerbils (Meriones unguiculatus) under three experimental conditions: normal labyrinths intact, acutely following unilateral labyrinthine lesion, and four to seven weeks following labyrinthine lesion. The number of type II neurons detected contralateral to the lesion was greatly reduced both in the acutely hemilabyrinthectomized animals and following compensation. The gain of the responses was depressed bilaterally acutely following the lesion. A greater reduction in response gain was noted in cells contralateral to the lesion. The gain of the contralateral type II responses increased with time such that in the compensated animal bilaterally symmetric gains were recorded. While the significant changes which occur in the gain of type II neurons with recovery from peripheral vestibular lesions can largely be attributed to type I neurons on the other side of the midline, changes in type I neurons were not entirely reflected in the type II population. The spontaneous activity of type II neurons did not undergo any significant changes following the labyrinthine lesion. We present a model utilizing the dynamic responses to estimate the functional recovery of commissural connections in compensated animals. The overall gain of the contralateral type I to ipsilateral type I commissural polysynaptic pathway appears to improve, while the efficacy in the reverse direction remains depressed, suggesting that modifications in commissural connections, particularly involving the type II to type I connections within the MVN on the injured side, mediate aspects of behavioral recovery.