MST responses to pursuit across optic flow with motion parallax.

Self-movement creates the patterned visual motion of optic flow with a focus of expansion (FOE) that indicates heading direction. During pursuit eye movements, depth cues create a retinal flow field that contains multiple FOEs, potentially complicating heading perception. Paradoxically, human heading perception during pursuit is improved by depth cues. We have studied medial superior temporal (MST) neurons to see whether their heading selectivity is also improved under these conditions. The responses of 134 MST neurons were recorded during the presentation of optic flow stimuli containing one or three speed-defined depth planes. During pursuit, multiple depth-plane stimuli evoked larger responses (71% of neurons) and stronger heading selectivity (70% of neurons). Responses to the three speed-defined depth-planes presented separately showed that most neurons (54%) preferred one of the planes. Responses to multiple depth-plane stimuli were larger than the averaged responses to the three component planes, suggesting enhancing interactions between depth-planes. Thus speed preferences create selective responses to one of many depth-planes in the retinal flow field. The presence of multiple depth-planes enhances those responses. These properties might improve heading perception during pursuit and contribute to relative depth perception.

MST neuronal responses to heading direction during pursuit eye movements.

As you move through the environment, you see a radial pattern of visual motion with a focus of expansion (FOE) that indicates your heading direction. When self-movement is combined with smooth pursuit eye movements, the turning of the eye distorts the retinal image of the FOE but somehow you still can perceive heading. We studied neurons in the medial superior temporal area (MST) of monkey visual cortex, recording responses to FOE stimuli presented during fixation and smooth pursuit eye movements. Almost all neurons showed significant changes in their FOE selective responses during pursuit eye movements. However, the vector average of all the neuronal responses indicated the direction of the FOE during both fixation and pursuit. Furthermore, the amplitude of the net vector increased with increasing FOE eccentricity. We conclude that neuronal population encoding in MST might contribute to pursuit-tolerant heading perception.

Eye position signals in the abducens and oculomotor nuclei of monkeys during ocular convergence.

Many neurons in oculomotor pathways encode signals related to eye position. For example, motoneurons in the third, fourth, and sixth cranial nuclei discharge at highly regular rates during fixation intervals. During fixations of far targets, their tonic discharge is linearly related to conjugate eye position. Previous studies provided evidence that premotor cells in brainstem pathways also encoded conjugate eye position. McConville et al. (this volume), however, measured eye movements during binocular fixations when the eyes were converged and concluded that the position signal encoded by premotor position-vestibular-pause (PVP) cells in the vestibular nuclei is related to monocular (right or left) eye position rather than to conjugate eye position. This surprising relationship would not have been noticed in earlier studies that measured the movements of only one eye (using a single eye coil) or that measured only the conjugate movements of the two eyes (using bitemporal EOG electrodes). How general a feature of oculomotor signal processing is this finding? In this paper, we re-examine the eye position signal in abducens and oculomotor neurons when the movements of the two eyes are conjugate and when they are disjunctive and therefore disassociated. The data suggest that abducens neurons (AMNs and AINs) and oculomotor neurons (putative medial rectus motoneurons), unlike PVP cells, are not monocular but encode mixtures of right and left eye position signals.

Magnocellular or parvocellular lesions in the lateral geniculate nucleus of monkeys cause minor deficits of smooth pursuit eye movements.

The effects of unilateral LGN lesions, made with ibotenic acid, on smooth pursuit eye movements were studied in two monkeys (Macaca nemestrina). Both monkeys received unilateral magnocellular (M-) layer lesions 18 months before the study and one monkey received a parvocellular (P-) lesion during the study on the side opposite the magnocellular lesion. The lesions did not affect the accuracy of saccades to stationary or moving targets, but the latencies of saccades to targets in the M-layer lesioned hemifields were significantly longer. Neither M- nor P-layer lesions affected the earliest interval (0-50 msec) of pursuit initiation, but during later intervals (50-150 msec), eye acceleration was less for pursuit initiation in the lesioned hemifield compared to the control hemifield. M-layer lesions created larger deficits in ocular acceleration than P-layer lesions. All deficits, however, were relatively small and accurate pursuit speeds were achieved near the time of the initial "catch-up" saccade. If both M and P layers representing the same part of the visual field were destroyed, the monkey was unable to locate the target or initiate smooth pursuit eye movements. We conclude that smooth pursuit initiation receives contributions from both the M- and P-layers of the LGN and either of these inputs can support pursuit initiation.