Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements

Abstract

Retinal image stability is essential for vision but may be degraded by head movements. The vestibulo-ocular reflex (VOR) compensates for passive perturbations of head position and is usually assumed to be the major neural mechanism for ocular stability. During our recent investigation of vestibular reflexes in guinea pigs free to move their heads (Shanidze et al. in Exp Brain Res, 2010), we observed compensatory eye movements that could not have been initiated either by vestibular or neck proprioceptive reflexes because they occurred with zero or negative latency with respect to head movement. These movements always occurred in association with self-generated (active) head or body movements and thus anticipated a voluntary movement. We found the anticipatory responses to differ from those produced by the VOR in two significant ways. First, anticipatory responses are characterized by temporal synchrony with voluntary head movements (latency approximately 1 versus approximately 7 ms for the VOR). Second, the anticipatory responses have higher gains (0.80 vs. 0.46 for the VOR) and thus more effectively stabilize the retinal image during voluntary head movements. We suggest that anticipatory responses act synergistically with the VOR to stabilize retinal images. Furthermore, they are independent of actual vestibular sensation since they occur in guinea pigs with complete peripheral vestibular lesions. Conceptually, anticipatory responses could be produced by a feed-forward neural controller that transforms efferent motor commands for head movement into estimates of the sensory consequences of those movements.

Fig. 1

Anticipatory eye movements that preserve retinal image stability occur in temporal synchrony with head movements. A. Example of self-generated head movements and eye movement responses. Upper black trace: eye-in-space (gaze) velocity; lower black trace: eye-in-head velocity; lower gray trace: head-in-space velocity. B. Portion of record shown in a (marked by arrow) with expanded gaze velocity scale. C. Waveform cross correlation of the data segment shown in a. The anticipatory response latency is the lag (−1 msec) at the maximum correlation. D. Linear regression analysis of eye-in-head and head-in-space velocities for the data segment shown in a. The regression slope is −0.95

Fig. 2

Two examples of anticipatory eye movements during self-generated rightward head movements. In both panels the uppermost traces are head (gray) and eye (black) position in space; 2^nd panel from top shows eye-in-head position (black); 3^rd panel from top shows head (gray) velocity in space and eye (black) velocity in relative to the head; 4^th panel from top shows eye velocity in space (black). The arrows indicate the anticipatory eye movement that precedes the rapid eye movement

Fig. 3

Cross correlation and regression analyses of the data segments illustrated in Fig. 2. A. Waveform correlation for the segment indicated by the arrow in Fig. 2a. The latency is −2 msec. B. Waveform correlation for the data segment that follows the rapid eye movement in Fig. 2A. The latency is 8 msec. C. Waveform correlation for the segment indicated by the arrow in Fig. 2B. The latency is −1 msec. D. Regression analysis for the segment indicated by the arrow in Fig. 2A. The regression slope is −0.75. E. Linear regression analysis for the segment that follows the rapid eye movement in Fig. 2A. The regression slope is −0.89. F. Regression analysis for the segment indicated by the arrow in Fig. 2B. The regression slope is −0.94

Fig. 4

A. Distribution of eye movement latencies (lags) associated with self-generated head movements. B. Distribution of regression slopes (compensatory gain) of eye versus head velocity associated with self-generated head movements. The “normalized count” is the count of items in each bin divided by the total number of counts

Fig. 5

Two examples of anticipatory eye movements in an animal 4 months after a complete bilateral vestibular lesion. A. Passive perturbation followed by an active head movement. B. Active head movement. Traces are ordered as in Fig. 2

Fig. 6

Distribution of anticipatory eye movement latencies (A) and regression slopes (gain, B) in 5 animals recorded 2 weeks after bilateral vestibular lesions. Upper half of each panel shows data from lesioned animals; lower half is control data

Fig. 7

Temporal synchrony of anticipatory eye movements with head movement improves retinal stability. A. Upper panel: head-in-space velocity (gray); eye-in-head velocity (black). Lower panel: eye-in-space (gaze) velocity (black) and simulated eye-in-space if the anticipatory response were delayed 7 msec (dotted trace). B. Regression analysis of eye and head velocity. Black dots, actual data; gray dots, delayed data

Fig. 8

Conceptual feed-forward model of proposed anticipatory eye movement mechanism. Details in text