Changes in eye position during fixation caused by inactivation of the rostral superior colliculus

During fixation of a visual target, gaze direction and target direction are normally aligned. The current dominant view holds that this behavior involves “fixation cells” that inhibit the generation of saccadic commands after the internal representations of target and gaze directions are matched in a common reference frame. An alternative view proposes that the alignment during fixation is accomplished by the collective effect of error signals. In particular, at the level of the brainstem, the direction of gaze may be determined by establishing a point of balance from the position error signals provided by neurons in both rostral superior colliculi (rSC). According to this hypothesis, local inactivation of one rSC should reduce or eliminate the generation of small contralesional saccades, thus leading to an ipsilesional offset in the scatter of eye position during fixation.

We have tested these predictions in the head-restrained monkey trained to fixate targets of various sizes (radius: 0.1°, 1°, 2°) before and after muscimol injection (0.5µl, 5µg/µl) in various sectors within the rSC. Preliminary results collected in one monkey (5 injection sites) confirm an ipsilesional offset in the scatter of eye position during fixation after inactivating the rSC. The offset had a size that increased with target size and, as expected from the topography of the SC map, was downward when the injection was made in its medial border and upward when it was made more laterally. Despite these alterations in starting eye position, the accuracy of subsequent saccades made to more peripheral targets was largely unaffected.

These results indicate that the direction of the line of sight during fixation is defined by the population activity of rSC neurons, each of which represents a particular position error, similar to the way that saccade endpoints are defined by the population activity of neurons in more caudal regions of the SC. Thus, there is no need for a reference direction in order to compute target and gaze directions; “zero error” is implemented by the symmetry of projections from the fovea and parafoveal region toward saccade related territories. Irregularities in these projections could be compensated at the level of premotor neurons by gain adjustments from the oculomotor cerebellum.

Reference:

Goffart, L., Hafed, Z.M., Dill, N. and Krauzlis, R.J. Changes in eye position during fixation caused by inactivation of the rostral superior colliculus. Society for Neuroscience Abstract, 2006.

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