Cited by 179Motor Control and AdaptationVisual perception and processing mechanismsVestibular and auditory disorders

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Memory of Learning Facilitates Saccadic Adaptation in the Monkey

Open access
Kojima, Yoshiko, Iwamoto, Yoshiki, Yoshida, Kaoru·2004·The Journal of Neuroscience

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.

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Crossref · 10.1523/jneurosci.1741-04.2004

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Figures

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 saccadeselicited by horizontal 10° target steps in one direction. C , Summaryofsevenparadigms used in the present study.
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 saccadeselicited by horizontal 10° target steps in one direction. C , Summaryofsevenparadigms used in the present study.CC-BY-NC-SA · From the PDF
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 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.CC-BY-NC-SA · From the PDF
Image 3
CC-BY-NC-SA · From the PDF
Figure4 A , Gain change profile of a zero-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).
Figure4 A , Gain change profile of a zero-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).CC-BY-NC-SA · From the PDF
Figure5 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. 3 B ). 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).
Figure5 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. 3 B ). 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).CC-BY-NC-SA · From the PDF
Figure6 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).
Figure6 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).CC-BY-NC-SA · From the PDF
Figure7 A , Gain change profiles of dark gain-increase experiments in monkey K ( Aa ) and monkeyI( 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.
Figure7 A , Gain change profiles of dark gain-increase experiments in monkey K ( Aa ) and monkeyI( 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.CC-BY-NC-SA · From the PDF
Figure8 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 memoryamplifiestheeffectofplasticityprocessoccurringinthecerebellarcortex,resultinginacceleratedadaptation. b , Increases anddecreasesingaindependonseparateplasticitymechanismsinthecerebellarcortex. 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.
Figure8 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 memoryamplifiestheeffectofplasticityprocessoccurringinthecerebellarcortex,resultinginacceleratedadaptation. b , Increases anddecreasesingaindependonseparateplasticitymechanismsinthecerebellarcortex. 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.CC-BY-NC-SA · From the PDF

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Citations

Cites

Research works printed but not linked: 5

  1. 2003, Soc Neurosci Abstr, 29, 441.7
  2. 2003, Neurosci Res, 46, S159
  3. 2002, Soc Neurosci Abstr, 28, 265.2
  4. 2003, Neurosci Res, 46, S49
  5. 2003, Soc Neurosci Abstr, 29, 79.1

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Metadata

Authors
Kojima, Y., Iwamoto, Y., & Yoshida, K.
Affiliations
University of Tsukuba (JP)
Corresponding author
Iwamoto, Yoshiki
Venue
The Journal of Neuroscience
Published
2004-08-25
Volume
24
Issue
34
Pages
7531-7539
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2096184857
Cited by
179
References
31
Citations by year
2026: 3 · 2025: 8 · 2024: 5 · 2023: 9 · 2022: 6 · 2021: 15 · 2020: 19 · 2019: 18 · 2018: 5 · 2017: 5 · 2016: 7 · 2015: 13 · 2014: 11 · 2013: 8 · 2012: 5
FWCI
2.35
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Japan Society for the Promotion of Science (13680894)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Motor Control and Adaptation
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Life Sciences › Neuroscience › Neurology › Vestibular and auditory disorders
Keywords
saccadic adaptation, motor learning, visual deprivation
MeSH terms
Adaptation, Ocular, Animals, Learning, Macaca mulatta, Male, Memory, Saccades

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