Experience-dependent changes in cerebellar contributions to motor sequence learning

Doyon, Julien; Song, Allen W.; Karni, Avi; Lalonde, François; Adams, Michelle M.; Ungerleider, Leslie G.

doi:10.1073/pnas.022615199

Cited by 412 publications

(311 citation statements)

References 39 publications

(46 reference statements)

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“…In contrast, the role of the SMA during the learning of skillful movement sequences remains less well understood. The SMA was activated in some imaging studies when subjects performed previously learned movement sequences compared with new sequences (Doyon et al 2002;Grafton et al 1998;Jenkins et al 1994), but this activation was not consistently observed in other studies (Rauch et al 1995(Rauch et al , 1997Sakai et al 1998Sakai et al , 2002Willingham et al 2002). The reason for this discrepancy is not known, although it might be related to the differences in the behavioral paradigms.…”

Section: Introductionmentioning

confidence: 42%

“…Previous lesion and imaging studies have suggested that the SMA plays a role in the retrieval and execution of previously learned movement sequences (Doyon et al 2002;Goldberg 1985;Grafton et al 1995Grafton et al , 1998Hazeltine et al 1997;Jenkins et al 1994;van Mier et al 1998). However, lesion studies tend to focus disproportionately on the functional deficit resulting from a particular lesion rather than on functions that might be normally supported by a given cortical area but spared by the lesion due to redundancy or recovery.…”

Section: Comparison To Previous Studiesmentioning

confidence: 97%

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Activity in the Supplementary Motor Area Related to Learning and Performance During a Sequential Visuomotor Task

Lee

Quessy

2003

Journal of Neurophysiology

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Lee, Daeyeol, and Stephan Quessy. Activity in the supplementary motor area related to learning and performance during a sequential visuomotor task. J Neurophysiol 89: 1039 -1056, 2003. First published October 30, 2002 10.1152/jn.00638.2002. Monkeys were trained in a serial reaction time task to produce hand movements according to changing locations of visual targets. In most trials, targets followed the same sequence repeatedly, whereas in other trials targets were presented in random locations or switched unpredictably between two alternative sequences. Single-unit activity was recorded from the caudal supplementary motor area (SMA-proper). Based on the activity associated with random movement sequences, effects of hand position and movement direction were evaluated. Activity was influenced by the hand position in ϳ60% of the neurons, and the movement direction influenced the activity of 51% of the neurons. In addition, 37 and 71% of SMA neurons displayed nonstationarity in their activity across successive movements within a given trial and across trials, respectively. Such nonstationarity in the ongoing neural activity and the effects of performance-related variables were evaluated using a regression model and separated from learningrelated activity changes. About a third of SMA neurons displayed gradual changes in neural activity related to experience with a movement sequence across trials. Furthermore, about a quarter of SMA neurons showed similar changes within individual trials. When the individual movements included in the frequently repeated movement sequences were introduced unexpectedly, learning-related changes in neural activity were reduced, indicating that many SMA neurons changed their activity in relation to the learning of particular movement sequences. These results suggest that the pattern of neural activity in the cortical network involved in the control of movement sequences can be modified continuously by experience.

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Section: Introductionmentioning

confidence: 42%

Section: Comparison To Previous Studiesmentioning

confidence: 97%

Activity in the Supplementary Motor Area Related to Learning and Performance During a Sequential Visuomotor Task

Lee

Quessy

2003

Journal of Neurophysiology

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“…Notwithstanding, increased cerebellar activation was reported during movement imagination [Decety et al, 1994;Jueptner et al, 1997], preparation [Deiber et al, 1996;Krams et al, 1998], and observation with the aim to imitate [Grèzes et al, , 1999, although the highest activations are usually found during actual movement execution [Deiber et al, 1996;Jueptner et al, 1997;Krams et al, 1998]. Cerebellum plays also a significant role in the early phases of acquisition and planning of motor sequences [Doyon et al, 2002], and is known to participate in a wide variety of cognitive and emotional processes [e.g., see Marien et al, 2001;Middleton and Strick, 1998;Rapoport et al, 2000;Salman, 2002]. Moreover, a modular organization of internal models of tool manipulation has been recently reported in the cerebellum using fMRI [Imamizu et al, 2003], extending the predictions of the MOSAIC computational model [Haruno et al, 2001;Wolpert and Kawato, 1998] from to the "motor" to the "cognitive" cerebellum.…”

Section: Innervatory Patternsmentioning

confidence: 99%

Imaging a cognitive model of apraxia: The neural substrate of gesture‐specific cognitive processes

Peigneux

Linden

Garraux

et al. 2004

Human Brain Mapping

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Abstract:The present study aimed to ascertain the neuroanatomical basis of an influential neuropsychological model for upper limb apraxia [Rothi LJ, et al. The Neuropsychology of Action. 1997. Hove, UK: Psychology Press]. Regional cerebral blood flow was measured in healthy volunteers using H 2 15O PET during performance of four tasks commonly used for testing upper limb apraxia, i.e., pantomime of familiar gestures on verbal command, imitation of familiar gestures, imitation of novel gestures, and an action-semantic task that consisted in matching objects for functional use. We also re-analysed data from a previous PET study in which we investigated the neural basis of the visual analysis of gestures. First, we found that two sets of discrete brain areas are predominantly engaged in the imitation of familiar and novel gestures, respectively. Segregated brain activation for novel gesture imitation concur with neuropsychological reports to support the hypothesis that knowledge about the organization of the human body mediates the transition from visual perception to motor execution when imitating novel gestures [Goldenberg Neuropsychologia 1995;33:63-72]. Second, conjunction analyses revealed distinctive neural bases for most of the gesture-specific cognitive processes proposed in this cognitive model of upper limb apraxia. However, a functional analysis of brain imaging data suggested that one single memory store may be used for "to-be-perceived" and "to-be-produced" gestural representations, departing from Rothi et al.'s proposal. Based on the above considerations, we suggest and discuss a revised model for upper limb apraxia that might best account for both brain imaging findings and neuropsychological dissociations reported in the apraxia literature.

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“…It remains a puzzle, however, as to which conditions lead to reduced or enhanced activations as a result of perceptual learning. It should be noted that brain imaging studies of motor skill learning have also reported both types of effect (Karni et al, 1995;Doyon et al, 2002;Wu et al, 2004), and no hypothesis has yet provided a sufficient explanation for this unresolved issue.…”

Section: Changes In Visual Cortex Activation During Perceptual Learningmentioning

confidence: 99%

Activations in Visual and Attention-Related Areas Predict and Correlate with the Degree of Perceptual Learning

Mukai¹,

Kim²,

Fukunaga³

et al. 2007

J. Neurosci.

151

131

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Repeated experience with a visual stimulus can result in improved perception of the stimulus, i.e., perceptual learning. To understand the underlying neural mechanisms of this process, we used functional magnetic resonance imaging to track brain activations during the course of training on a contrast discrimination task. Based on their ability to improve on the task within a single scan session, subjects were separated into two groups: "learners" and "nonlearners." As learning progressed, learners showed progressively reduced activation in both visual cortex, including Brodmann's areas 18 and 19 and the fusiform gyrus, and several cortical regions associated with the attentional network, namely, the intraparietal sulcus (IPS), frontal eye field (FEF), and supplementary eye field. Among learners, the decrease in brain activations in these regions was highly correlated with the magnitude of performance improvement. Unlike learners, nonlearners showed no changes in brain activations during training. Learners showed stronger activation than nonlearners during the initial period of training in all these brain regions, indicating that one could predict from the initial activation level who would learn and who would not. In addition, over the course of training, the functional connectivity between IPS and FEF in the right hemisphere with early visual areas was stronger for learners than nonlearners. We speculate that sharpened tuning of neuronal representations may cause reduced activation in visual cortex during perceptual learning and that attention may facilitate this process through an interaction of attention-related and visual cortical regions.

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Experience-dependent changes in cerebellar contributions to motor sequence learning

Cited by 412 publications

References 39 publications

Activity in the Supplementary Motor Area Related to Learning and Performance During a Sequential Visuomotor Task

Activity in the Supplementary Motor Area Related to Learning and Performance During a Sequential Visuomotor Task

Imaging a cognitive model of apraxia: The neural substrate of gesture‐specific cognitive processes

Activations in Visual and Attention-Related Areas Predict and Correlate with the Degree of Perceptual Learning

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