Superior colliculus neurons mediate the dynamic characteristics of saccades

Abstract

1. The locus of activity within the superior colliculus (SC) is related to the desired displacement of the eye. Current hypotheses suggest that the location of this locus of activity determines the amplitude of the saccade and that the level of activity at this locus determines eye velocity. We present evidence that suggests that, although the locus determines the amplitude of the saccade, the level of activity in the colliculus encodes dynamic motor error (the difference between desired and current eye displacement). 2. We categorized 86 neurons in the intermediate and deep layers of the superior colliculus of two rhesus monkeys by their activity in relation to the end of saccadic eye movements. In 36% of the cells (n = 31), activity was completely cut off by the end of the saccade (clipped cells). For 53% of cells (n = 46), the major burst of activity ceased by the end of the saccade, but activity continued for 30-100 ms after the end of the movement (partially clipped cells). The remaining 10% of the cells (n = 9) had no clear burst of activity (unclipped cells) but rather had activity that increased gradually before the saccade and then slowly decreased for up to 100 ms after the saccade. These categories were part of a continuum of cell types rather than discrete classes of cells. 3. We first determined whether this new categorization of cells revealed a special relation between the discharge of clipped and partially clipped cells and saccadic amplitude and peak velocity. As expected, we found a steady increase in spike count as saccadic amplitude increased up to the center of the movement field, and an increase in peak spike discharge as peak velocity increased up to a maximum radial eye velocity. Variability in the cell discharge was substantially greater than the variability of saccadic amplitude or peak velocity. We concluded that these single point or averaged measures did not reveal any new functional relationship of these cells. 4. We then examined the relationship of the temporal pattern of discharge of clipped and partially clipped cells to instantaneous changes in radial error and radial velocity. There was a monotonic decay in spike discharge with declining radial error. In contrast, there was a complex, multivalued relationship between spike discharge and radial velocity; collicular cells produced two different values of spike discharge for the same velocity, one during acceleration and the other during deceleration of the eye during a saccade.(ABSTRACT TRUNCATED AT 400 WORDS)

Perisaccadic Compression Correlates with Saccadic Peak Velocity: Differential Association of Eye Movement Dynamics with Perceptual Mislocalization Patterns

“…On the one hand, it may suggest that the level of perisaccadic perceptual compression varies with the strength of the corresponding saccadic motor command: saccadic peak velocities correlate with average firing rates of burst neurons recorded in the superior colliculi (Waitzman et al, 1991) and the pontomedullary reticular formation (Van Gisbergen et al, 1981). The superior colliculi and downstream structures provide an important source of reafferent signals that are fed back to frontal and parietal oculomotor areas via thalamic relay nuclei (Buttner-Ennever and Henn, 1976;Sommer and Wurtz, 2002).…”

Intrinsic Reference Frames of Superior Colliculus Visuomotor Receptive Fields during Head-Unrestrained Gaze Shifts

“…Investigations of saccade dynamics during SC stimulation and recordings have suggested that the SC does influence velocity (Waitzman et al, 1991;Guitton, 1992;Van Opstal et al, 1995;Munoz et al, 1996). Head-restrained studies that dissociated target location from gaze kinematics by varying initial eye position (Sparks and Mays, 1980) or perturbing eye muscles have suggested that SC neurons correlate best to the former, rather than the latter.…”

Reversible inactivation of macaque frontal eye field

“…20), which repre- sents where the eye should go (Robinson 1975;van Gisbergen et al 1981;Jürgens et al 1981;Scudder 1988;van Gisbergen and van Opstal 1989;Waitzman et al 1991). E d needs to be a sustained signal: it not only represents where to go but also drives the saccade.…”