Characteristics of Saccadic Gain Adaptation in Rhesus Macaques

Abstract

We adapted the saccadic gain (saccadic amplitude/target step amplitude) by requiring monkeys to track a small spot that stepped to one side by 5, 10, or 15 degrees and then, during the initial targeting saccade, jumped either forward or backward by a fixed percentage of the initial step. Saccadic gain increased or decreased, respectively, as a function of the number of adapting saccades made in that direction. The relation between gain and the number of adapting saccades was fit with an exponential function, yielding an asymptotic gain and a rate constant (the number of saccades to achieve 63% of the total change in gain). Backward intrasaccadic target jumps of 15, 30, and 50% of the initial target step reduced the asymptotic gain by an average of 12.2, 23.1, and 36.4%, respectively, with average rate constants of 163, 368, and 827 saccades, respectively. During 50% backward jumps, some saccades, especially those to larger target steps, became slower and lasted longer. Forward intrasaccadic jumps of 30% increased the asymptotic gain by 23.3% (average rate constant of 1,178 saccades). After we had caused adaptation, we induced recovery of gain toward normal by requiring the animal to track target steps without intrasaccadic jumps. Recovery following forward adaptation required about one third fewer saccades than the preceding gain increase. Recovery following backward adaptation required about the same average number of saccades as the preceding gain decrease. The first saccades of recovery were slightly less adapted than the last saccades of adaptation, suggesting that a small part of adaptation might have been strategic. After 50% backward jumps had reduced saccadic gain, the hypometric primary saccades during recovery were followed by hypometric corrective saccades, suggesting that they too had been adapted. When saccades of only one size underwent gain reduction, saccades to target steps of other amplitudes showed much less adaptation. Also, saccades in the direction opposite to that adapted were not adapted. Gain reductions endured if an adapted animal was placed in complete darkness for 20 h. These data indicate that saccadic gain adaptation is relatively specific to the adapted step and does not produce parametric changes of all saccades. Furthermore, adaptation is not a strategy, but involves enduring neuronal reorganization in the brain. We suggest that this paradigm engages mechanisms that determine saccadic gain in real life and therefore offers a reversible means to study their neuronal substrate.

Discharge of Monkey Nucleus Reticularis Tegmenti Pontis Neurons Changes During Saccade Adaptation

“…In general, the amplitude change produced by forward adaptation (15.4 Ϯ 3.8%) was less than that produced by backward adaptation as has been reported by others (e.g., Straube et al 1997). During a behavioral increase in saccade amplitude, we found no statistically significant changes in the number of spikes calculated by the comparison of either the sets of preand postadaptation trials (n ϭ 10) or the first and last 20 adaptation trials (n ϭ 2).…”

“…If thresholds were too low, we used target amplitudes that before adaptation were associated with large differences in discharge. We attempted to decrease saccade amplitude for open field neurons because amplitude increases are smaller and more difficult to induce (e.g., Straube et al 1997) so that associated changes in firing would be more difficult to discern. If the unit had a closed field, we mostly (11/14 neurons) attempted to increase saccade amplitude.…”

Head-Unrestrained Gaze Adaptation in the Rhesus Macaque

“…Furthermore, in accordance with previous accounts of head-restrained saccadic adaptation (Bahcall and Kowler 2000;Deubel 1991;Miller et al 1981;Noto et al 1999;Robinson et al 2003;Scudder et al 1998;Straube et al 1997), backward adaptation was larger in magnitude than forward adaptation in response to the same postsaccadic visual error. Phillips and colleagues (1997) showed that head-restrained saccadic adaptation transfers to head-unrestrained gaze shifts.…”

“…During visual orienting behaviors, this type of adaptation has been studied by introducing visual errors near the end of saccadic eye movements (Deubel 1987(Deubel , 1991Deubel et al 1986;McLaughlin 1967;Miller et al 1981;Noto et al 1999;Robinson et al 2003;Scudder et al 1998;Semmlow et al 1987;Straube et al 1997). When the head is prevented from moving, a shift in target location triggered by the beginning of a saccade leads initially to a visual error at the end of the movement.…”

“…When the head is prevented from moving, a shift in target location triggered by the beginning of a saccade leads initially to a visual error at the end of the movement. As similar trials are repeated, the amplitude of the movements made to the first target location change (increasing or decreasing) so that the error at the end of the movement is reduced (Deubel 1987(Deubel , 1991Deubel et al 1986;McLaughlin 1967;Miller et al 1981;Noto et al 1999;Robinson et al 2003;Scudder et al 1998;Semmlow et al 1987;Straube et al 1997). Changes in saccade amplitude follow a roughly exponential time course with "rate constants" around 30 -60 saccades in humans (Albano 1996;Deubel 1987;Deubel et al 1986;Frens and vanOpstal 1994) and between 100 and 800 saccades in monkeys (Straube et al 1997).…”