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Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system.

Panouillères M, Urquizar C, Salemme R, Pélisson D - PLoS ONE (2011)

Bottom Line: We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways.Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task.These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.

View Article: PubMed Central - PubMed

Affiliation: INSERM U1028, CNRS UMR5292, Lyon Neuroscience Research Center, IMPACT (Integrative, Multisensory, Perception, Action and Cognition) Team and University Lyon 1, Lyon, France. muriel.panouilleres@inserm.fr

ABSTRACT
When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.

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Time-course of the adaptation of reactive and voluntary saccades.Mean gain change is represented as a function of the blocks of trials and superimposed for the different post-saccadic durations of jumped target in the mask condition (grey background – A, B) and no-mask condition (white background – C, D), for reactive (A, C) and voluntary (B, D) saccades adaptation. Mean gain change was calculated across the 5 subjects of each experimental session. Gray lines indicate the gain changes for the shortest target durations (dashed lines: 15 ms – solid lines: 50 ms) and black lines indicate the gain changes for the longest target durations (dashed lines: 100 ms – solid lines: 800 ms). The blocks of trials are: pre-adaptation (pre), adaptation blocks with an intra-saccadic step of 25% of initial target eccentricity (a25, b25) or of 40% (c40, d40) and post-adaptation (post). Error bars are SEMs. Significant differences of gain changes between the target durations are indicated by * (p<0.05), ** (p<0.01) and *** (p<0.001).
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pone-0017329-g002: Time-course of the adaptation of reactive and voluntary saccades.Mean gain change is represented as a function of the blocks of trials and superimposed for the different post-saccadic durations of jumped target in the mask condition (grey background – A, B) and no-mask condition (white background – C, D), for reactive (A, C) and voluntary (B, D) saccades adaptation. Mean gain change was calculated across the 5 subjects of each experimental session. Gray lines indicate the gain changes for the shortest target durations (dashed lines: 15 ms – solid lines: 50 ms) and black lines indicate the gain changes for the longest target durations (dashed lines: 100 ms – solid lines: 800 ms). The blocks of trials are: pre-adaptation (pre), adaptation blocks with an intra-saccadic step of 25% of initial target eccentricity (a25, b25) or of 40% (c40, d40) and post-adaptation (post). Error bars are SEMs. Significant differences of gain changes between the target durations are indicated by * (p<0.05), ** (p<0.01) and *** (p<0.001).

Mentions: The time-courses of the gain changes are presented for reactive and voluntary saccades in Figures 2A and 2B, respectively. The saccadic adaptation is shown superimposed for the different target durations. The depicted increase of gain changes across successive blocks of trials revealed a progressive decrease of gain during the adaptation phase. For reactive saccade adaptation, the gain changes seemed to be lower for the shortest target duration than for other target durations, but only in the last adaptation block and in the post-adaptation block. Conversely, the adaptation of voluntary saccades is strongly impaired for the two shortest target durations (15 and 50 ms), throughout all the adaptation phase and the post-adaptation block. Thus, the adaptation seems to depend on the target duration, but also on the category of saccades. To quantify this, the mean gain changes were submitted to a three-way ANOVA testing the “block” (pre, …post), “saccade type” (reactive vs voluntary), and “target duration” factors (15 ms vs 50 ms vs 100 ms vs 800 ms). Significant effects of all three factors were found (F[5,432] = 63.8, p<0.001; F[1,432] = 24.1, p<0.001 and F[3,432] = 28, p<0.001 respectively). A strong interaction between the “target duration” and the “saccade type” factors was also found (F[3,432] = 10.2, p<0.001), and the interaction between “target duration” and “block” factors just reached significance (F[15,432] = 1.7, p = 0.05). The effect of the “block” factor resulted from a progressive decrease of saccade gain in the adaptation and post-adaptation blocks for all target durations and for the two types of saccades (Figures 2A and 2B). The other results of the ANOVA indicated that these adaptive gain changes depended both on saccade type and on target duration. For the shortest durations of target (15 and 50 ms), the gain of reactive saccades showed a larger decrease than the gain of voluntary saccades for the last two blocks of adaptation (c40 and d40) and the post-adaptation block (“after-effect”) (post-hoc Fisher's LSD test, p<0.05). In contrast, no significant difference between the gain changes of reactive and voluntary saccades was highlighted for the long target durations (100 ms and 800 ms). For reactive saccades, the gain changes differed between the longest (800 ms) and the shortest (15 ms) target durations only for the last block of adaptation and the post-adaptation block (post-hoc Fisher's LSD test, p<0.05). Contrary to this, for voluntary saccades, gain changes differed between the two shortest durations (15 ms and 50 ms) and the two longest durations (100 ms and 800 ms) of jumped target for all adaptation blocks but a25 and for the post-adaptation block (post-hoc Fisher's LSD test, p<0.01 and p<0.001).


Sensory processing of motor inaccuracy depends on previously performed movement and on subsequent motor corrections: a study of the saccadic system.

Panouillères M, Urquizar C, Salemme R, Pélisson D - PLoS ONE (2011)

Time-course of the adaptation of reactive and voluntary saccades.Mean gain change is represented as a function of the blocks of trials and superimposed for the different post-saccadic durations of jumped target in the mask condition (grey background – A, B) and no-mask condition (white background – C, D), for reactive (A, C) and voluntary (B, D) saccades adaptation. Mean gain change was calculated across the 5 subjects of each experimental session. Gray lines indicate the gain changes for the shortest target durations (dashed lines: 15 ms – solid lines: 50 ms) and black lines indicate the gain changes for the longest target durations (dashed lines: 100 ms – solid lines: 800 ms). The blocks of trials are: pre-adaptation (pre), adaptation blocks with an intra-saccadic step of 25% of initial target eccentricity (a25, b25) or of 40% (c40, d40) and post-adaptation (post). Error bars are SEMs. Significant differences of gain changes between the target durations are indicated by * (p<0.05), ** (p<0.01) and *** (p<0.001).
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3044175&req=5

pone-0017329-g002: Time-course of the adaptation of reactive and voluntary saccades.Mean gain change is represented as a function of the blocks of trials and superimposed for the different post-saccadic durations of jumped target in the mask condition (grey background – A, B) and no-mask condition (white background – C, D), for reactive (A, C) and voluntary (B, D) saccades adaptation. Mean gain change was calculated across the 5 subjects of each experimental session. Gray lines indicate the gain changes for the shortest target durations (dashed lines: 15 ms – solid lines: 50 ms) and black lines indicate the gain changes for the longest target durations (dashed lines: 100 ms – solid lines: 800 ms). The blocks of trials are: pre-adaptation (pre), adaptation blocks with an intra-saccadic step of 25% of initial target eccentricity (a25, b25) or of 40% (c40, d40) and post-adaptation (post). Error bars are SEMs. Significant differences of gain changes between the target durations are indicated by * (p<0.05), ** (p<0.01) and *** (p<0.001).
Mentions: The time-courses of the gain changes are presented for reactive and voluntary saccades in Figures 2A and 2B, respectively. The saccadic adaptation is shown superimposed for the different target durations. The depicted increase of gain changes across successive blocks of trials revealed a progressive decrease of gain during the adaptation phase. For reactive saccade adaptation, the gain changes seemed to be lower for the shortest target duration than for other target durations, but only in the last adaptation block and in the post-adaptation block. Conversely, the adaptation of voluntary saccades is strongly impaired for the two shortest target durations (15 and 50 ms), throughout all the adaptation phase and the post-adaptation block. Thus, the adaptation seems to depend on the target duration, but also on the category of saccades. To quantify this, the mean gain changes were submitted to a three-way ANOVA testing the “block” (pre, …post), “saccade type” (reactive vs voluntary), and “target duration” factors (15 ms vs 50 ms vs 100 ms vs 800 ms). Significant effects of all three factors were found (F[5,432] = 63.8, p<0.001; F[1,432] = 24.1, p<0.001 and F[3,432] = 28, p<0.001 respectively). A strong interaction between the “target duration” and the “saccade type” factors was also found (F[3,432] = 10.2, p<0.001), and the interaction between “target duration” and “block” factors just reached significance (F[15,432] = 1.7, p = 0.05). The effect of the “block” factor resulted from a progressive decrease of saccade gain in the adaptation and post-adaptation blocks for all target durations and for the two types of saccades (Figures 2A and 2B). The other results of the ANOVA indicated that these adaptive gain changes depended both on saccade type and on target duration. For the shortest durations of target (15 and 50 ms), the gain of reactive saccades showed a larger decrease than the gain of voluntary saccades for the last two blocks of adaptation (c40 and d40) and the post-adaptation block (“after-effect”) (post-hoc Fisher's LSD test, p<0.05). In contrast, no significant difference between the gain changes of reactive and voluntary saccades was highlighted for the long target durations (100 ms and 800 ms). For reactive saccades, the gain changes differed between the longest (800 ms) and the shortest (15 ms) target durations only for the last block of adaptation and the post-adaptation block (post-hoc Fisher's LSD test, p<0.05). Contrary to this, for voluntary saccades, gain changes differed between the two shortest durations (15 ms and 50 ms) and the two longest durations (100 ms and 800 ms) of jumped target for all adaptation blocks but a25 and for the post-adaptation block (post-hoc Fisher's LSD test, p<0.01 and p<0.001).

Bottom Line: We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways.Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task.These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.

View Article: PubMed Central - PubMed

Affiliation: INSERM U1028, CNRS UMR5292, Lyon Neuroscience Research Center, IMPACT (Integrative, Multisensory, Perception, Action and Cognition) Team and University Lyon 1, Lyon, France. muriel.panouilleres@inserm.fr

ABSTRACT
When goal-directed movements are inaccurate, two responses are generated by the brain: a fast motor correction toward the target and an adaptive motor recalibration developing progressively across subsequent trials. For the saccadic system, there is a clear dissociation between the fast motor correction (corrective saccade production) and the adaptive motor recalibration (primary saccade modification). Error signals used to trigger corrective saccades and to induce adaptation are based on post-saccadic visual feedback. The goal of this study was to determine if similar or different error signals are involved in saccadic adaptation and in corrective saccade generation. Saccadic accuracy was experimentally altered by systematically displacing the visual target during motor execution. Post-saccadic error signals were studied by manipulating visual information in two ways. First, the duration of the displaced target after primary saccade termination was set at 15, 50, 100 or 800 ms in different adaptation sessions. Second, in some sessions, the displaced target was followed by a visual mask that interfered with visual processing. Because they rely on different mechanisms, the adaptation of reactive saccades and the adaptation of voluntary saccades were both evaluated. We found that saccadic adaptation and corrective saccade production were both affected by the manipulations of post-saccadic visual information, but in different ways. This first finding suggests that different types of error signal processing are involved in the induction of these two motor corrections. Interestingly, voluntary saccades required a longer duration of post-saccadic target presentation to reach the same amount of adaptation as reactive saccades. Finally, the visual mask interfered with the production of corrective saccades only during the voluntary saccades adaptation task. These last observations suggest that post-saccadic perception depends on the previously performed action and that the differences between saccade categories of motor correction and adaptation occur at an early level of visual processing.

Show MeSH
Related in: MedlinePlus