Memory of learning facilitates saccadic adaptation in the monkey

Abstract

A motor learning mechanism called saccadic adaptation ensures accuracy of saccades throughout life despite growth, aging, and some pathologies of the oculomotor plant or nervous system. The present study investigates effects of preceding adaptation on the speed of subsequent adaptation during single experiments. Adaptive changes in gain (movement size divided by target eccentricity) were induced by intrasaccadic step (ISS) of the target. After the gain was altered (control block), we reversed the direction of ISS to bring the gain back to approximately 1.0 (recovery). We then reversed ISS direction again to induce another adaptation (test block). Analyses revealed that the gain changed at a higher rate in the early part of test adaptation than in the corresponding part of control. After approximately 100-300 saccades in the test block, adaptation slowed down. The gain value at which adaptation slowed was correlated with the gain achieved in the control. We further examined effects of a 30 min intervention inserted between recovery and test blocks. When zero-visual-error trials ( approximately 700 saccades) were repeated during this period, the rate of test adaptation was similar to that of control. In contrast, when the animal was deprived of visual inputs during this period, test adaptation was still influenced by preceding learning. We conclude that a memory of previous learning remains during recovery to facilitate subsequent adaptation and that such a memory does not disappear merely with time but is erased actively by repeated zero-error movements. Our results, which cannot be explained by a single mechanism, suggest that the saccadic system is equipped with more than one plasticity process.

Figure 1.

A, B, Illustration of standard double-reversal paradigm for gain-increase adaptation (A) and gain-decrease adaptation (B). First, adaptation was induced by 35% forward (A) or 35% backward (B) ISS (control block). The direction of ISS was reversed to bring the gain back to ∼1.0 (recovery block). We then reversed the ISS direction again and induced a gain change (test block) using the ISS of the same size and direction as in the control block. We adapted saccade selicited by horizontal 10° target steps in one direction. C, Summary of seven paradigms used in the present study.

Figure 2.

A, Gain change profile of a gain-increase experiment with linear regression lines fitted for the first 150 saccades of control and test blocks. The slope of test adaptation was larger than that of control. B, Gain change profile of a gain-decrease experiment with similar regression lines. Note the steeper slope of test adaptation. C, D, Summaries of gain change rate for gain-increase experiments (C) and gain-decrease experiments (D). Test adaptation has a significantly higher rate than control adaptation except for gain-decrease experiments in monkey I. Data shown in A and B are indicated by small horizontal arrows in C and D, respectively.

Figure 3.

Slowing of adaptation. A, Gain change profiles for two gain-increase experiments, in which accelerated adaptation appears to end abruptly to produce inflections (arrows) on the fitted curves. Control adaptation in Aa exhibits a higher gain than that in Ab. Correspondingly, the gain at facilitation end in test adaptation in Aa is higher than in Ab. B, Estimation of facilitation end gain for the experiment in Aa. Profile of instantaneous rate of gain change, slopes of linear regression line for 150 saccade moving window plotted as a function of saccade number (top). Slope of test adaptation (black line) was initially larger but decreases beyond that of control adaptation (gray line). The crossing point was regarded as facilitation end. Facilitation end gain was calculated as the average gain of 50 saccades distributed about facilitation end (bottom). C, Relationship between facilitation end gain and control final gain. There was a significant positive correlation between the two parameters both in gain-increase adaptation (left) with p < 0.05, r = 0.86, and n = 6 for monkey K and p < 0.05, r = 0.77, and n = 7 for monkey I, and in gain-decrease adaptation (right) with p < 0.05, r = 0.76, and n = 7 for monkey K and p < 0.01, r = 1.00, and n = 4 for monkey I. Data shown in Aa and Ab are indicated by small horizontal arrows (labeled a and b, respectively) in C.

Figure 4.

A, Gain change profile of azero-error gain-decrease experiment with linear regression lines fitted for the first 150 saccades of the control and test blocks. B, Summary of all experiments with this paradigm in two monkeys. There was no significant difference in gain change rate between the test and control. Data shown in A is indicated by a small horizontal arrow in B (monkey K).

Figure 5.

A, Gain change profile of a dark gain-decrease experiment with linear regression lines fitted for the first 150 saccades of the control and test blocks. The slope of test adaptation is steeper than that of control. B, Summary of all experiments with this paradigm in two monkeys. Test adaptation has a significantly larger rate than control adaptation. Data shown in A are indicated by a small horizontal arrow in B (monkey K). C, Slowing of test adaptation seen as an inflection (arrow) on the fitting curve. D, Relationship between facilitation end gain and control final gain. The facilitation end gain was calculated by the same method as for standard paradigm data (Fig. 3B). There was a significant positive correlation between the two parameters in monkey K (left; p < 0.01; r = 0.88; n = 7). The relationship did not reach a significant level in monkey I (right; p = 0.1; r = 0.90; n = 4). Data shown in C are indicated by a small horizontal arrow in D (monkey K).

Figure 6.

A, Gain change profile of a zero-error gain-increase experiment with linear regression lines fitted for the first 150 saccades of the control and test blocks. B, Summary of all experiments with this paradigm in two monkeys. There was no significant difference in gain change rate between the test and control. Data shown in A are indicated by a small horizontal arrow in B (monkey K).

Figure 7.

A, Gain change profiles of dark gain-increase experiments in monkey K (Aa) and monkey I (Ab). Test adaptation starts with a gain that is higher than the gain at recovery end. Height of open arrows indicates this jump in gain, which is 0.08 and 0.16 for Aa and Ab, respectively. B, Gain change profile of a dark no-ISS experiment. In contrast to A, the no-ISS test block starts with a gain that is similar to the gain at recovery end. C, A jump in gain is shown as a bar chart with SD for each paradigm in the two monkeys. Positive values represent gain changes in the same direction as the ISS. The jump in the dark gain-increase paradigm (asterisk) was significantly larger than that in any other paradigm in both animals.

Figure 8.

Possible mechanisms for facilitated adaptation. A, Postulated sites of plasticity in two general schemes. a, A memory of learning forms in the cerebellar nucleus during control adaptation and remains during recovery. During test adaptation, this memory amplifies the effect of plasticity process occurring in the cerebellar cortex, resulting in accelerated adaptation. b, Increases and decreases in gain depend on separate plasticity mechanisms in the cerebellar cortex. B, Schematic illustrations of how the two oppositely directed mechanisms, assumed in Ab, might produce acceleration and subsequent slowing of adaptation observed in the present study. a, Standard gain-decrease paradigm. In the early phase of test adaptation, reactivation of gain-decrease process (broken line) combined with deactivation of gain increase process (gray solid line) produces accelerated gain change (black solid line). When gain increase process recovers fully to baseline, it stops being deactivated and can no longer contribute to overall gain change, resulting in slowing of adaptation (inflection on the gain curve). b, Zero-error paradigm. Erasure of memory is realized by simultaneous deactivation of the two mechanisms to baseline. c, Dark paradigm. Both mechanisms remain partially activated during the dark block, exhibiting acceleration and slowing in the test block.