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Visual error is the stimulus for saccade gain adaptation
Cognitive Brain Research 12 (2001) 301–305 www.elsevier.com / locate / bres
Research report
Visual error is the stimulus for saccade gain adaptation Christopher T. Noto*, Farrel R. Robinson Department of Biological Structure and Regional Primate Research Center, University of Washington, Seattle, WA 98195 -7420, USA Accepted 24 April 2001
Abstract Saccade accuracy is fundamental to clear vision. The brain maintains saccade accuracy by altering commands for saccades that are consistently inaccurate. For example, saccades that consistently overshoot their targets gradually become smaller. The signal that drives the adaptation of saccade size is not well understood. Previous reports propose that corrective movements and visual errors, both generated after inaccurate saccades, could be responsible for a change in saccade size. Here we show that we can elicit normal reductions in saccade size while eliciting few or no correction saccades. These normal reductions in saccade size indicate that visual errors, not correction saccades, drive the adaptation of saccades. 2001 Elsevier Science B.V. All rights reserved. Theme: Neural basis of behavior Topic: Learning and memory: systems and functions Keywords: Eye movement; Saccade adaptation; Visual error; Correction saccade
1. Introduction If saccades (voluntary rapid eye movements) repeatedly miss targets in the same direction they adapt (i.e., they gradually change to become more accurate). The signal that drives saccade adaptation is not yet established. Some [1,2] suggested that the drive might depend on the occurrence of an error signal generated by a correction saccade that is made to foveate the intended target after an errant saccade. These corrective movements could signal the size and direction of the error, information that could then drive the adaptation mechanism to modify subsequent movements. Though it is plausible that correction saccades account for the change in saccade size during saccade adaptation, recent data indicate that they account for at most half the change in size. Wallman and Fuchs [3] used intrasaccadic back steps of a target to adaptively reduce saccade size in monkeys. They also reduced the number of correction saccades made during adaptation by modifying the usual procedure. About 200 ms after the target moved during the
*Corresponding author. Tel.: 11-206-221-3366; fax: 11-206-5431524. E-mail address: [email protected] (C.T. Noto).
saccade, it returned to the position that evoked the initial saccade. This pattern of target movement elicited very few backward correction saccades and resulted in a clear reduction in the size of a monkey’s saccades. The size of this reduction was only about half the size of the reduction elicited in separate adaptation sessions during which the target remained at the position to which it moved during the saccade (i.e., at the back stepped location). Wallman and Fuchs argue that because significant adaptation occurs despite a dramatic reduction in the number of appropriate correction saccades, correction saccades are not very influential in reducing saccade gain. They propose that visual error signal, the difference between eye and target position at the end of the saccade, is more influential. According to their view, their adaptation procedure that elicited few correction saccades caused less adaptation than conventional adaptation because the procedure presented two conflicting error signals following each saccade. The first visual error occurred when the target was at the location it moved to during the saccade. The second occurred 200 ms later when the target returned to the position that elicited the saccade. The data from Wallman and Fuchs also support an alternative interpretation. It is possible that correction saccades are necessary for |50% of the size of the adaptation. This could be the reason that nearly eliminating
0926-6410 / 01 / $ – see front matter 2001 Elsevier Science B.V. All rights reserved. PII: S0926-6410( 01 )00062-3
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C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
them as Wallman and Fuchs did causes only |50% of the size reduction elicited by conventional adaptation. In the study described here, we manipulated target movement to elicit saccade adaptation with a minimum number of corrective movements. Our procedure also eliminated conflicting visual errors after saccades. Thus, if correction saccades play no role in saccade adaptation, our procedure should result in reductions that are the same size as conventional adaptations. Alternatively, if the execution of correction saccades is necessary for half of the reduction in saccade size, our procedure will cause half the normal amount of change caused during conventional adaptations. We found that adaptation without correction saccades or conflicting visual errors reduces saccade size to levels similar to experiments in which correction saccades occur normally. This result supports the proposal that visual error signals alone can drive adaptive changes in saccade size. Our results also support Wallman and Fuchs’ proposal that conflicting visual errors reduce adaptation size. In a second experiment we tested this explicitly by measuring the effect of conflicting errors on adaptation.
2. Methods
2.1. Subjects and visual stimulus Two rhesus macaques (monkey M and monkey B) that demonstrated robust saccade adaptation participated in these experiments. We trained each monkey to use single saccades to look directly at a target spot after it moved. The 0.38 target was produced with a laser diode and was projected onto a tangent screen 57 cm in front of the monkey. Two computer-controlled mirror galvanometers intersecting the spot’s image set the position of the target on the screen. The spot never moved more than 208 from the center of the screen. We monitored eye position with the search coil technique [4,5] and used small acrylic appliances attached to the skull to hold the head steady during training and data collection. We implanted both the search coil and the acrylic appliances in a single aseptic surgery. A week after surgery we began training each monkey to use saccades to follow target movements with an accuracy of 618. The target moved about 1 s after the monkey fixated it at a particular position. The monkey received a dollop of applesauce as a reward if it successfully followed the target for 2.5–3.5 s. Training was complete when our subjects could make saccades to track accurately (i.e., within 18) .2500 target steps within a single training session (i.e., |1.5 h). The Institutional Animal Care and Use Committee approved all training and surgical procedures at the University of Washington. Housing and veterinary care at the Washington Regional Primate Research Center meets or exceeds all standards in the National Institutes of Health
‘‘Guide for the Care and Use of Laboratory Animals’’ as well as the standards of the Institute of Laboratory Animal Resources and the American Association for Accreditation of Laboratory Animal Care.
2.2. Conventional adaptation experiments In conventional adaptation experiments we reduced saccade size by moving the target back toward its starting position during each saccade [6–9]. We measured the change in saccade size as a change in gain. Saccade gain is the common measure of saccade accuracy and is equal to the size of the saccade divided by the target’s step size. We elicited 108 saccades at the start of adaptation by moving the target spot rapidly 108 to the left or right along the horizontal meridian. During the saccade that the monkey made to follow the target, the computer moved the target 38 back in the opposite direction. This back step occurred when the saccade first reached a velocity above |758 / s and then decelerated to |308 / s. In each experimental session we presented back stepping targets during both rightward and leftward saccades. Adaptation in one direction does not influence the gain of saccades in the opposite direction [6,8–12] so we treated the simultaneous adaptation of rightward and leftward saccades as two separate experiments. We measured the changes that occurred during four conventional adaptations in each monkey, i.e., separate left and right adaptations in each of two adaptation sessions. We recorded the session until adaptation appeared to have gone to completion (995–1329 saccades).
2.3. Modified adaptation experiments As in conventional adaptation, we reduced the gain of the monkey’s rightward and leftward saccades in the same adaptation session. Also, we employed the same saccade velocity criteria to trigger a 38 target back step. However, in the modified adaptation procedure the target remained illuminated for only 90 ms after it stepped back. Then the computer extinguished it for 500 ms. When the target became visible again it had moved to a new location 108 from its position after the back step. This pattern of target movement and illumination caused monkeys to reliably make saccades to the initial target position but elicited few or no correction saccades to the target at its back stepped location. We measured four modified adaptations in each monkey, i.e., separate left and right adaptations in each of two adaptation sessions. In the modified adaptation sessions we recorded 1305–1492 saccades.
2.4. Reward By the time that we collected data from a monkey, it was very well trained to look directly at the target to
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
receive a dollop of applesauce (the reward for performing the task) from a feeding tube near its mouth. During experiments, we gave the monkeys applesauce at the end of |50% of the trials whether or not they fixated the target. Even without being required to foveate the target for a reward our monkeys reliably made saccades toward the target in both the conventional and modified adaptation experiments.
2.5. Data collection and analysis Conventional and modified adaptation experiments were interleaved for monkey B. Monkey B’s experiments were completed within about 1 week. Modified adaptation experiments were preceded by conventional experiments in monkey M. Experiments were run over a period of about 1 month, each was separated by about 1 week. Neither animal appeared to carry changes in amplitude between experimental sessions (i.e., the decrease from one experiment did not influence the adaptation occurring in the next session). Before each conventional or modified adaptation session we used a Vetter PCM and a modified video cassette recorder to record 22–33 leftward and rightward preadaptation saccades made to normal (i.e., not back-stepping) 108 horizontal target steps. We recorded similar numbers of leftward and rightward post-adaptation saccades after each conventional and modified adaptation session. We digitized, at 1 kHz, voltages representing eye and target movement during pre-adaptation and postadaptation. We analyzed the digitized data with an interactive program that allowed the user to mark each saccade and the target movement that elicited it. The program calculated the gain of every saccade. To determine if gain reduction occurred during a particular adaptation, we compared the gains of pre- and post-adaptation saccades with a t-test for means with equal variance. We considered P#0.05 to be significant. Further, we calculated the percentage of gain change in both conventional and modified adaptations using the formula: Percent gain change (mean pre-adaptation gain 2 single post-adaptation gain) 5 ]]]]]]]]]]]]]]]] mean pre-adaptation gain 3 100 This formula has been used elsewhere to provide the percentage change from the mean pre-adaptation gain for each post-adaptation saccade [13,14]. Determining the percentage change of each post-adaptation saccade allowed us compare saccades from different sessions with statistical tests and also to characterize the variability of adapted saccade gain.
303
3. Results
3.1. Conventional adaptation experiments As expected from previous work in both monkeys [9,15] and humans [7,8], the two monkeys in this study significantly reduced the size of their saccades during each of the four conventional adaptations (each P,0.001). Also, they made corrective movements to capture the target following every saccade during adaptation (i.e., corrective movements followed 100% of the targeting saccades during adaptation). The average gain reduction for conventional adaptation was 18.2% in monkey M and 23.0% in monkey B (Fig. 1, conventional adaptation).
3.2. Modified adaptation In four modified adaptation sessions, monkey M made 0, 5, 6, and 38 correction saccades (i.e., following 0, 0.7, 0.8, and 5% of its initial saccades, respectively, for an average of 1.6%). Monkey B made 0, 7, 29, and 45 correction saccades (after 0, 1.1, 4.0, and 6.4% of its saccades, for an average of 3%). All four modified adaptations in both monkeys significantly reduced saccade gain (each P, 0.001), by an average of 15.2% in monkey M and 21.3% in monkey B (Fig. 1, modified adaptation). This amount of gain decrease was achieved in approximately the same number of saccades as conventional adaptation. To determine if minimizing the number of correction saccades impaired adaptation we compared the gain change caused by each conventional adaptation with that caused by modified adaptation using a one-way ANOVA. Neither monkey showed a consistent difference. Of the 16 possible comparisons in monkey B (four conventional adaptations compared to four modified adaptations), 11 indicated no significant difference, three indicated that the modified adaptation was smaller than the conventional adaptation, and two showed that modified adaptations were larger than normal (for each significant difference, P, 0.004). In monkey M, 15 comparisons indicated no significant difference and one comparison indicated that modified adaptation was smaller than normal (for each significant difference, P,0.001). Thus, the severe reduction in the number of corrective movements (from 100% during conventional adaptation to |2% during modified adaptation) did little or nothing to disrupt gain reduction.
3.3. Conflicting errors If correction saccades have little influence on adaptation size, why did Wallman and Fuchs [3] observe a |50% reduction in adaptation when they drastically reduced the number of correction saccades? They propose that the conflicting visual error signals following each saccade with reduced size impaired the performance of the adaptation mechanism. If this were true, other conditions that provide
304
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
Fig. 1. Summary of the average percentage of change in gain. The four conventional adaptation experiments (filled circles) and the four modified adaptation experiments (open circles) in monkey M and monkey B are shown. As well, overall average percentage of change in gain for conventional (filled squares) and modified experiments (open squares) are indicated. Error bars are6S.D.
conflicting error signals would similarly cause abnormally small changes in gain. We tested this during 20 adaptation sessions with monkey M. In these experiments, the target stepped back after only some saccades. We varied the proportion of back stepping targets triggered by saccades in different experiments. In this way we provide conflicting signals, i.e., ‘no adaptation necessary’ when the target
did not step back during a saccade and ‘reduce saccade size’ when it did. We found that, decreasing the proportion of back stepping target movements decreased the amount of gain change caused by the adaptation. For example, a regimen containing equal numbers of intermixed back stepping and non-back-stepping targets produced just 63% of the gain change caused by adaptations containing only back-stepping targets (Fig. 2). Though the errors created in Wallman and Fuchs’s experiments and our own differ slightly (i.e., two errors per saccade and ‘alternating’ single errors, respectively), both Wallman’s data and our own suggest that conflicting information about saccade accuracy interferes with gain reductions.
4. Discussion
Fig. 2. The percentage of change in gain caused by adaptations presenting different proportions of target movements with intrasaccadic back-steps. Open circles are the percentage change in gain for individual adaptations. Filled squares are average values. The line running through the data is a third order polynomial fit ( y5 20.00003x 3 10.0037x 2 1 0.392x15.085, R 2 50.76). The small gain reductions observed in adaptations containing no back-steps are a normal consequence of requiring monkeys to make many saccades [16].
The major finding of this study is that nearly eliminating the correction saccades that occur during saccade adaptation had little or no effect on a monkey’s ability to reduce its saccade gain. This finding strongly supports the proposal that consistent visual errors drive saccade adaptation. We also show that conflicting error signals result in a reduction of gain proportional to the number of each type of error. Based on these two experiments, the 50% reduction in adaptation observed by Wallman and Fuchs [3] when they eliminated most of all correction saccades almost certainly resulted from the conflicting visual error signals present in their procedure — not from the absence or presence of correction saccades.
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
Acknowledgements We thank Dr. Albert F. Fuchs for generously supplying the resources without which this work would have been impossible. This study was supported by NIH grants RR00166 and EY10578.
References [1] J.E. Albano, W.M. King, Rapid adaptation of saccadic amplitude in humans and monkeys, Invest. Ophthalmol. Vis. Sci. 8 (1989) 1883– 1893. [2] N. Schweighofer, M.A. Arbib, P.F. Dominey, A model of the cerebellum in the adaptive control of saccadic gain. I. The model and its biological substrate, Biol. Cybernet 75 (1996) 19–28. [3] J. Wallman, A.F. Fuchs, Saccadic gain modification: visual error drives motor adaptation, J. Neurophysiol. 80 (1998) 2405–2416. [4] A.F. Fuchs, D.A. Robinson, A method for measuring horizontal and vertical eye movements chronically in the monkey, J. Appl. Physiol. 21 (1966) 1068–1070. [5] D.A. Robinson, A method of measuring eye movement using a scleral search coil in a magnetic field, IEEE Trans. Biomed. Electron. BME 10 (1963) 137–145. [6] H. Deubel, W. Wolf, G. Hauske, Adaptive gain control of saccadic eye movements, Hum. Neurobiol. 5 (1986) 245–253.
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[7] S.C. McLaughlin, Parametric adjustment in saccadic eye movements, Percept. Psychophys. 2 (1967) 359–362. [8] J.M. Miller, A. Anstis, W.B. Templeton, Saccadic plasticity: parametric adaptive control of retinal feedback, J. Exp. Psycyol. 7 (1981) 356–366. [9] A. Straube, A.F. Fuchs, S. Usher, F. Robinson, Characteristics of saccadic gain adaptation in rhesus macaques, J. Neurophysiol. 77 (1997) 874–895. [10] J.E. Albano, Adaptive changes in saccade amplitude: oculocentric or orbitocentric mapping, Vision Res. 36 (1996) 2087–2098. [11] M.A. Frens, A.J. Van Opstal, Monkey superior colliculus activity during short term saccadic adaptation, Brain Res Bull. 43 (1997) 473–483. [12] G.E. Weisfeld, Parametric adjustment to a shifting target alternating with saccades to a stationary reference point, Psychonom. Sci. 28 (1972) 72–74. [13] F.R. Robinson, C.T. Noto, S. Watanabe, Effect of visual background on scaccadic adaptation in monkeys, Vis. Res. 40 (2000) 2359– 2367. [14] J.L. Shafer, C.T. Noto, A.F. Fuchs, Temporal characteristics of error signal driving saccadeic gain adaptation in the Macaque monkey, J. Neurophysiol. 84 (2000) 88–95. [15] C.T. Noto, S. Watanabe, A.F. Fuchs, Characteristics of simian adaptation fields produced by behavioral changes in saccade size and direction, J. Neurophysiol. 81 (1999) 2798–2813. [16] A. Straube, F.R. Robinson, A.F. Fuchs, Decrease in saccadic performance after many visually guided saccadic eye movements in monkeys, Invest. Ophthalmol. 38 (1998) 2810–2816.
Research report
Visual error is the stimulus for saccade gain adaptation Christopher T. Noto*, Farrel R. Robinson Department of Biological Structure and Regional Primate Research Center, University of Washington, Seattle, WA 98195 -7420, USA Accepted 24 April 2001
Abstract Saccade accuracy is fundamental to clear vision. The brain maintains saccade accuracy by altering commands for saccades that are consistently inaccurate. For example, saccades that consistently overshoot their targets gradually become smaller. The signal that drives the adaptation of saccade size is not well understood. Previous reports propose that corrective movements and visual errors, both generated after inaccurate saccades, could be responsible for a change in saccade size. Here we show that we can elicit normal reductions in saccade size while eliciting few or no correction saccades. These normal reductions in saccade size indicate that visual errors, not correction saccades, drive the adaptation of saccades. 2001 Elsevier Science B.V. All rights reserved. Theme: Neural basis of behavior Topic: Learning and memory: systems and functions Keywords: Eye movement; Saccade adaptation; Visual error; Correction saccade
1. Introduction If saccades (voluntary rapid eye movements) repeatedly miss targets in the same direction they adapt (i.e., they gradually change to become more accurate). The signal that drives saccade adaptation is not yet established. Some [1,2] suggested that the drive might depend on the occurrence of an error signal generated by a correction saccade that is made to foveate the intended target after an errant saccade. These corrective movements could signal the size and direction of the error, information that could then drive the adaptation mechanism to modify subsequent movements. Though it is plausible that correction saccades account for the change in saccade size during saccade adaptation, recent data indicate that they account for at most half the change in size. Wallman and Fuchs [3] used intrasaccadic back steps of a target to adaptively reduce saccade size in monkeys. They also reduced the number of correction saccades made during adaptation by modifying the usual procedure. About 200 ms after the target moved during the
*Corresponding author. Tel.: 11-206-221-3366; fax: 11-206-5431524. E-mail address: [email protected] (C.T. Noto).
saccade, it returned to the position that evoked the initial saccade. This pattern of target movement elicited very few backward correction saccades and resulted in a clear reduction in the size of a monkey’s saccades. The size of this reduction was only about half the size of the reduction elicited in separate adaptation sessions during which the target remained at the position to which it moved during the saccade (i.e., at the back stepped location). Wallman and Fuchs argue that because significant adaptation occurs despite a dramatic reduction in the number of appropriate correction saccades, correction saccades are not very influential in reducing saccade gain. They propose that visual error signal, the difference between eye and target position at the end of the saccade, is more influential. According to their view, their adaptation procedure that elicited few correction saccades caused less adaptation than conventional adaptation because the procedure presented two conflicting error signals following each saccade. The first visual error occurred when the target was at the location it moved to during the saccade. The second occurred 200 ms later when the target returned to the position that elicited the saccade. The data from Wallman and Fuchs also support an alternative interpretation. It is possible that correction saccades are necessary for |50% of the size of the adaptation. This could be the reason that nearly eliminating
0926-6410 / 01 / $ – see front matter 2001 Elsevier Science B.V. All rights reserved. PII: S0926-6410( 01 )00062-3
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C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
them as Wallman and Fuchs did causes only |50% of the size reduction elicited by conventional adaptation. In the study described here, we manipulated target movement to elicit saccade adaptation with a minimum number of corrective movements. Our procedure also eliminated conflicting visual errors after saccades. Thus, if correction saccades play no role in saccade adaptation, our procedure should result in reductions that are the same size as conventional adaptations. Alternatively, if the execution of correction saccades is necessary for half of the reduction in saccade size, our procedure will cause half the normal amount of change caused during conventional adaptations. We found that adaptation without correction saccades or conflicting visual errors reduces saccade size to levels similar to experiments in which correction saccades occur normally. This result supports the proposal that visual error signals alone can drive adaptive changes in saccade size. Our results also support Wallman and Fuchs’ proposal that conflicting visual errors reduce adaptation size. In a second experiment we tested this explicitly by measuring the effect of conflicting errors on adaptation.
2. Methods
2.1. Subjects and visual stimulus Two rhesus macaques (monkey M and monkey B) that demonstrated robust saccade adaptation participated in these experiments. We trained each monkey to use single saccades to look directly at a target spot after it moved. The 0.38 target was produced with a laser diode and was projected onto a tangent screen 57 cm in front of the monkey. Two computer-controlled mirror galvanometers intersecting the spot’s image set the position of the target on the screen. The spot never moved more than 208 from the center of the screen. We monitored eye position with the search coil technique [4,5] and used small acrylic appliances attached to the skull to hold the head steady during training and data collection. We implanted both the search coil and the acrylic appliances in a single aseptic surgery. A week after surgery we began training each monkey to use saccades to follow target movements with an accuracy of 618. The target moved about 1 s after the monkey fixated it at a particular position. The monkey received a dollop of applesauce as a reward if it successfully followed the target for 2.5–3.5 s. Training was complete when our subjects could make saccades to track accurately (i.e., within 18) .2500 target steps within a single training session (i.e., |1.5 h). The Institutional Animal Care and Use Committee approved all training and surgical procedures at the University of Washington. Housing and veterinary care at the Washington Regional Primate Research Center meets or exceeds all standards in the National Institutes of Health
‘‘Guide for the Care and Use of Laboratory Animals’’ as well as the standards of the Institute of Laboratory Animal Resources and the American Association for Accreditation of Laboratory Animal Care.
2.2. Conventional adaptation experiments In conventional adaptation experiments we reduced saccade size by moving the target back toward its starting position during each saccade [6–9]. We measured the change in saccade size as a change in gain. Saccade gain is the common measure of saccade accuracy and is equal to the size of the saccade divided by the target’s step size. We elicited 108 saccades at the start of adaptation by moving the target spot rapidly 108 to the left or right along the horizontal meridian. During the saccade that the monkey made to follow the target, the computer moved the target 38 back in the opposite direction. This back step occurred when the saccade first reached a velocity above |758 / s and then decelerated to |308 / s. In each experimental session we presented back stepping targets during both rightward and leftward saccades. Adaptation in one direction does not influence the gain of saccades in the opposite direction [6,8–12] so we treated the simultaneous adaptation of rightward and leftward saccades as two separate experiments. We measured the changes that occurred during four conventional adaptations in each monkey, i.e., separate left and right adaptations in each of two adaptation sessions. We recorded the session until adaptation appeared to have gone to completion (995–1329 saccades).
2.3. Modified adaptation experiments As in conventional adaptation, we reduced the gain of the monkey’s rightward and leftward saccades in the same adaptation session. Also, we employed the same saccade velocity criteria to trigger a 38 target back step. However, in the modified adaptation procedure the target remained illuminated for only 90 ms after it stepped back. Then the computer extinguished it for 500 ms. When the target became visible again it had moved to a new location 108 from its position after the back step. This pattern of target movement and illumination caused monkeys to reliably make saccades to the initial target position but elicited few or no correction saccades to the target at its back stepped location. We measured four modified adaptations in each monkey, i.e., separate left and right adaptations in each of two adaptation sessions. In the modified adaptation sessions we recorded 1305–1492 saccades.
2.4. Reward By the time that we collected data from a monkey, it was very well trained to look directly at the target to
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
receive a dollop of applesauce (the reward for performing the task) from a feeding tube near its mouth. During experiments, we gave the monkeys applesauce at the end of |50% of the trials whether or not they fixated the target. Even without being required to foveate the target for a reward our monkeys reliably made saccades toward the target in both the conventional and modified adaptation experiments.
2.5. Data collection and analysis Conventional and modified adaptation experiments were interleaved for monkey B. Monkey B’s experiments were completed within about 1 week. Modified adaptation experiments were preceded by conventional experiments in monkey M. Experiments were run over a period of about 1 month, each was separated by about 1 week. Neither animal appeared to carry changes in amplitude between experimental sessions (i.e., the decrease from one experiment did not influence the adaptation occurring in the next session). Before each conventional or modified adaptation session we used a Vetter PCM and a modified video cassette recorder to record 22–33 leftward and rightward preadaptation saccades made to normal (i.e., not back-stepping) 108 horizontal target steps. We recorded similar numbers of leftward and rightward post-adaptation saccades after each conventional and modified adaptation session. We digitized, at 1 kHz, voltages representing eye and target movement during pre-adaptation and postadaptation. We analyzed the digitized data with an interactive program that allowed the user to mark each saccade and the target movement that elicited it. The program calculated the gain of every saccade. To determine if gain reduction occurred during a particular adaptation, we compared the gains of pre- and post-adaptation saccades with a t-test for means with equal variance. We considered P#0.05 to be significant. Further, we calculated the percentage of gain change in both conventional and modified adaptations using the formula: Percent gain change (mean pre-adaptation gain 2 single post-adaptation gain) 5 ]]]]]]]]]]]]]]]] mean pre-adaptation gain 3 100 This formula has been used elsewhere to provide the percentage change from the mean pre-adaptation gain for each post-adaptation saccade [13,14]. Determining the percentage change of each post-adaptation saccade allowed us compare saccades from different sessions with statistical tests and also to characterize the variability of adapted saccade gain.
303
3. Results
3.1. Conventional adaptation experiments As expected from previous work in both monkeys [9,15] and humans [7,8], the two monkeys in this study significantly reduced the size of their saccades during each of the four conventional adaptations (each P,0.001). Also, they made corrective movements to capture the target following every saccade during adaptation (i.e., corrective movements followed 100% of the targeting saccades during adaptation). The average gain reduction for conventional adaptation was 18.2% in monkey M and 23.0% in monkey B (Fig. 1, conventional adaptation).
3.2. Modified adaptation In four modified adaptation sessions, monkey M made 0, 5, 6, and 38 correction saccades (i.e., following 0, 0.7, 0.8, and 5% of its initial saccades, respectively, for an average of 1.6%). Monkey B made 0, 7, 29, and 45 correction saccades (after 0, 1.1, 4.0, and 6.4% of its saccades, for an average of 3%). All four modified adaptations in both monkeys significantly reduced saccade gain (each P, 0.001), by an average of 15.2% in monkey M and 21.3% in monkey B (Fig. 1, modified adaptation). This amount of gain decrease was achieved in approximately the same number of saccades as conventional adaptation. To determine if minimizing the number of correction saccades impaired adaptation we compared the gain change caused by each conventional adaptation with that caused by modified adaptation using a one-way ANOVA. Neither monkey showed a consistent difference. Of the 16 possible comparisons in monkey B (four conventional adaptations compared to four modified adaptations), 11 indicated no significant difference, three indicated that the modified adaptation was smaller than the conventional adaptation, and two showed that modified adaptations were larger than normal (for each significant difference, P, 0.004). In monkey M, 15 comparisons indicated no significant difference and one comparison indicated that modified adaptation was smaller than normal (for each significant difference, P,0.001). Thus, the severe reduction in the number of corrective movements (from 100% during conventional adaptation to |2% during modified adaptation) did little or nothing to disrupt gain reduction.
3.3. Conflicting errors If correction saccades have little influence on adaptation size, why did Wallman and Fuchs [3] observe a |50% reduction in adaptation when they drastically reduced the number of correction saccades? They propose that the conflicting visual error signals following each saccade with reduced size impaired the performance of the adaptation mechanism. If this were true, other conditions that provide
304
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
Fig. 1. Summary of the average percentage of change in gain. The four conventional adaptation experiments (filled circles) and the four modified adaptation experiments (open circles) in monkey M and monkey B are shown. As well, overall average percentage of change in gain for conventional (filled squares) and modified experiments (open squares) are indicated. Error bars are6S.D.
conflicting error signals would similarly cause abnormally small changes in gain. We tested this during 20 adaptation sessions with monkey M. In these experiments, the target stepped back after only some saccades. We varied the proportion of back stepping targets triggered by saccades in different experiments. In this way we provide conflicting signals, i.e., ‘no adaptation necessary’ when the target
did not step back during a saccade and ‘reduce saccade size’ when it did. We found that, decreasing the proportion of back stepping target movements decreased the amount of gain change caused by the adaptation. For example, a regimen containing equal numbers of intermixed back stepping and non-back-stepping targets produced just 63% of the gain change caused by adaptations containing only back-stepping targets (Fig. 2). Though the errors created in Wallman and Fuchs’s experiments and our own differ slightly (i.e., two errors per saccade and ‘alternating’ single errors, respectively), both Wallman’s data and our own suggest that conflicting information about saccade accuracy interferes with gain reductions.
4. Discussion
Fig. 2. The percentage of change in gain caused by adaptations presenting different proportions of target movements with intrasaccadic back-steps. Open circles are the percentage change in gain for individual adaptations. Filled squares are average values. The line running through the data is a third order polynomial fit ( y5 20.00003x 3 10.0037x 2 1 0.392x15.085, R 2 50.76). The small gain reductions observed in adaptations containing no back-steps are a normal consequence of requiring monkeys to make many saccades [16].
The major finding of this study is that nearly eliminating the correction saccades that occur during saccade adaptation had little or no effect on a monkey’s ability to reduce its saccade gain. This finding strongly supports the proposal that consistent visual errors drive saccade adaptation. We also show that conflicting error signals result in a reduction of gain proportional to the number of each type of error. Based on these two experiments, the 50% reduction in adaptation observed by Wallman and Fuchs [3] when they eliminated most of all correction saccades almost certainly resulted from the conflicting visual error signals present in their procedure — not from the absence or presence of correction saccades.
C.T. Noto, F.R. Robinson / Cognitive Brain Research 12 (2001) 301 – 305
Acknowledgements We thank Dr. Albert F. Fuchs for generously supplying the resources without which this work would have been impossible. This study was supported by NIH grants RR00166 and EY10578.
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