Recovery of saccadic dysmetria following localized lesions in monkey superior colliculus

Abstract

Damage to the monkey superior colliculus (SC) produces deficits in the generation of saccadic eye movements. Recovery of the accuracy of saccades is rapid, but saccadic latency and peak velocity recover slowly or not at all. In the present experiments we revisited the issue of recovery of function following localized lesions of the SC using three methodological advances: implantation of wire recording electrodes into the SC for the duration of the experiment to ensure that we were recording from the same site on the SC map on successive days; quantification of changes in saccadic accuracy, latency, and velocity using a standard grid of target points in the visual field contralateral to the SC lesion; measurement of movement field size to quantitatively determine any changes following the lesion. We confirmed a decrease in saccadic accuracy following electrolytic lesions of the SC, and we found that this dysmetria recovered within about 4 days. Saccadic latency increased for saccades to the lesion area and this deficit persisted. Peak saccadic velocity decreased immediately after the lesion and decreased further during the 10 days to 2 weeks of the experiment. We found no indication of an expansion of the movement fields of neurons adjacent to the lesion area. This lack of reorganization suggests that movement field changes within the SC cannot mediate the recovery in accuracy of the saccade. The persistence of the latency and velocity deficits despite the recovery of amplitude deficits indicates that saccadic latency and peak velocity are dependent upon the SC whereas saccadic amplitude is not.

Blink amplitude but not saccadic hypometria indicates carriers of Parkin mutations

“…Saccade hypometria in PD subjects may be caused by an excitation of the substantia nigra pars reticulata (SNr), which, in turn, inhibits the SC that specifies the size and direction of a saccade [14]. Accordingly, saccadic hypometria is found in SC lesions in patients [15] but has not been confirmed as a persistent deficit in a recent animal SC lesion study [9]. By contrast, saccadic circuits downstream of the SC seemed to be spared because blink-saccade interaction in our subjects was normal, i.e., blinks physiologically decreased saccade velocity [19,20].…”

Monetary reward speeds up voluntary saccades

“…The previous neurophysiological studies have indicated that dopamine-modulated oculomotor neurons in the basal ganglia regulate saccades through the superior colliculus (Wurtz and Goldberg, 1972; Schiller et al, 1980; Hikosaka and Wurtz, 1983, 1985a,b; Lee et al, 1988; van Opstal and van Gisbergen, 1990; van Opstal et al, 1995; Kawagoe et al, 1998; Sato and Hikosaka, 2002; Soetedjo et al, 2002; Hanes et al, 2005; Matsumoto and Hikosaka, 2009; Yasuda et al, 2012). For example, the superior colliculus– which received direct inhibitory inputs from the basal ganglia– exhibited a pre-saccadic burst of activity with a peak discharge rate positively correlated with saccadic peak velocity (van Opstal and van Gisbergen, 1990; van Opstal et al, 1995; Soetedjo et al, 2002).…”

Dynamic Ensemble Coding of Saccades in the Monkey Superior Colliculus

“…Larger lesions (data not shown) produced hypometric saccades, such as observed after muscimol injections (Quaia et al 1998), because the total number of SC spikes failed to reach the threshold. We conjecture that this threshold is under adaptive control, which would account for the altered movement fields after short-term adaptation of saccades (Frens and Van Opstal 1998) and the rapid recovery of amplitude deficits after small electrolytic lesions of the SC (Hanes et al 2005).…”

“…The notion that each SC spike adds a tiny site-specific displacement vector to the movement command implies that eye velocity is not only influenced by the cell firing rates and their anatomical connection strengths with the brain stem, but also by the number of recruited cells. Indeed, it has been shown that when a subset of the active cell population is reversibly inactivated, saccade velocity is consistently reduced Lee et al 1988;Quaia et al 1998) and that these velocity deficits persist in the case of irreversible lesions (Hanes et al 2005). saccade endpoints with (green) and without (blue) lesion.…”