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Two distinct ipsilateral cortical representations for individuated finger movements.

Diedrichsen J, Wiestler T, Krakauer JW - Cereb. Cortex (2012)

Bottom Line: A second type of representation becomes evident in caudal premotor and anterior parietal cortices during bimanual actions.In these regions, ipsilateral actions are represented as nonlinear modulation of activity patterns related to contralateral actions, an encoding scheme that may provide the neural substrate for coordinating bimanual movements.We conclude that ipsilateral cortical representations change their informational content and functional role, depending on the behavioral context.

View Article: PubMed Central - PubMed

Affiliation: Institute of Cognitive Neuroscience, University College London, London, UK. j.diedrichsen@ucl.ac.uk

ABSTRACT
Movements of the upper limb are controlled mostly through the contralateral hemisphere. Although overall activity changes in the ipsilateral motor cortex have been reported, their functional significance remains unclear. Using human functional imaging, we analyzed neural finger representations by studying differences in fine-grained activation patterns for single isometric finger presses. We demonstrate that cortical motor areas encode ipsilateral movements in 2 fundamentally different ways. During unimanual ipsilateral finger presses, primary sensory and motor cortices show, underneath global suppression, finger-specific activity patterns that are nearly identical to those elicited by contralateral mirror-symmetric action. This component vanishes when both motor cortices are functionally engaged during bimanual actions. We suggest that the ipsilateral representation present during unimanual presses arises because otherwise functionally idle circuits are driven by input from the opposite hemisphere. A second type of representation becomes evident in caudal premotor and anterior parietal cortices during bimanual actions. In these regions, ipsilateral actions are represented as nonlinear modulation of activity patterns related to contralateral actions, an encoding scheme that may provide the neural substrate for coordinating bimanual movements. We conclude that ipsilateral cortical representations change their informational content and functional role, depending on the behavioral context.

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Pattern decomposition shows clear evidence for nonlinear bimanual tuning of voxels in the functionally defined bimanual ROI in pre- and postcentral gyri. (A) For the bimanual patterns, the variance estimate for the contralateral component is relatively strong and equivalent for uni- and bimanual movements. (B) The variance of the ipsilateral component effect is reduced for the bimanual movement compared with unimanual. However, a substantial interaction effect between ipsi- and contralateral fingers (white bar) is observed. (C) For contralateral fingers (red), there is a high correlation between the unimanual and bimanual pattern components of the same finger. For ipsilateral finger presses (blue), there is no systematic relationship. Box plots extend from the 25th to the 75th percentile. Whiskers indicate the full range of the data, with circle indicating data points that are further away from the median than 1.5 the times the box length (intraquartile range). (D) The classification accuracy for the ipsilateral finger during bimanual actions correlates with the size of the interaction effect. Values for the bimanual area within the left and right precentral and postcentral ROIs are shown for each participant. (E) Classification accuracy does not correlate with the size of a pattern component related to the ipsilateral main effect. Error bars indicate between-participant SE.
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BHS120F7: Pattern decomposition shows clear evidence for nonlinear bimanual tuning of voxels in the functionally defined bimanual ROI in pre- and postcentral gyri. (A) For the bimanual patterns, the variance estimate for the contralateral component is relatively strong and equivalent for uni- and bimanual movements. (B) The variance of the ipsilateral component effect is reduced for the bimanual movement compared with unimanual. However, a substantial interaction effect between ipsi- and contralateral fingers (white bar) is observed. (C) For contralateral fingers (red), there is a high correlation between the unimanual and bimanual pattern components of the same finger. For ipsilateral finger presses (blue), there is no systematic relationship. Box plots extend from the 25th to the 75th percentile. Whiskers indicate the full range of the data, with circle indicating data points that are further away from the median than 1.5 the times the box length (intraquartile range). (D) The classification accuracy for the ipsilateral finger during bimanual actions correlates with the size of the interaction effect. Values for the bimanual area within the left and right precentral and postcentral ROIs are shown for each participant. (E) Classification accuracy does not correlate with the size of a pattern component related to the ipsilateral main effect. Error bars indicate between-participant SE.

Mentions: Note that we did not use the ROI approach to make judgments of “whether” any regions significantly encoded finger presses in the first place. These tests were performed using multiple comparison corrections for the whole cortical surface. The functional ROI selection procedure was then performed to analyze “how” these regions encoded the finger presses. For example, we could compare within these ROIs between contra- and ipsilateral conditions for Experiment 1 and between contralateral, ipsilateral, unimanual, and bimanual conditions for Experiment 2. This is assured because these contrasts are orthogonal to the voxel-selection criterion, and the experimental design was fully balanced (Kriegeskorte et al. 2009). Also, any assessment of the correlation between left- and right-hand patterns can be made in an unbiased fashion, as the classification is performed independently for the 2 hands and selection is not biased toward specific patterns. For the decomposition analysis presented in Figure 7, we ensured through Monte-Carlo simulation that the selection criterion did not bias subsequent analyses.


Two distinct ipsilateral cortical representations for individuated finger movements.

Diedrichsen J, Wiestler T, Krakauer JW - Cereb. Cortex (2012)

Pattern decomposition shows clear evidence for nonlinear bimanual tuning of voxels in the functionally defined bimanual ROI in pre- and postcentral gyri. (A) For the bimanual patterns, the variance estimate for the contralateral component is relatively strong and equivalent for uni- and bimanual movements. (B) The variance of the ipsilateral component effect is reduced for the bimanual movement compared with unimanual. However, a substantial interaction effect between ipsi- and contralateral fingers (white bar) is observed. (C) For contralateral fingers (red), there is a high correlation between the unimanual and bimanual pattern components of the same finger. For ipsilateral finger presses (blue), there is no systematic relationship. Box plots extend from the 25th to the 75th percentile. Whiskers indicate the full range of the data, with circle indicating data points that are further away from the median than 1.5 the times the box length (intraquartile range). (D) The classification accuracy for the ipsilateral finger during bimanual actions correlates with the size of the interaction effect. Values for the bimanual area within the left and right precentral and postcentral ROIs are shown for each participant. (E) Classification accuracy does not correlate with the size of a pattern component related to the ipsilateral main effect. Error bars indicate between-participant SE.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3643717&req=5

BHS120F7: Pattern decomposition shows clear evidence for nonlinear bimanual tuning of voxels in the functionally defined bimanual ROI in pre- and postcentral gyri. (A) For the bimanual patterns, the variance estimate for the contralateral component is relatively strong and equivalent for uni- and bimanual movements. (B) The variance of the ipsilateral component effect is reduced for the bimanual movement compared with unimanual. However, a substantial interaction effect between ipsi- and contralateral fingers (white bar) is observed. (C) For contralateral fingers (red), there is a high correlation between the unimanual and bimanual pattern components of the same finger. For ipsilateral finger presses (blue), there is no systematic relationship. Box plots extend from the 25th to the 75th percentile. Whiskers indicate the full range of the data, with circle indicating data points that are further away from the median than 1.5 the times the box length (intraquartile range). (D) The classification accuracy for the ipsilateral finger during bimanual actions correlates with the size of the interaction effect. Values for the bimanual area within the left and right precentral and postcentral ROIs are shown for each participant. (E) Classification accuracy does not correlate with the size of a pattern component related to the ipsilateral main effect. Error bars indicate between-participant SE.
Mentions: Note that we did not use the ROI approach to make judgments of “whether” any regions significantly encoded finger presses in the first place. These tests were performed using multiple comparison corrections for the whole cortical surface. The functional ROI selection procedure was then performed to analyze “how” these regions encoded the finger presses. For example, we could compare within these ROIs between contra- and ipsilateral conditions for Experiment 1 and between contralateral, ipsilateral, unimanual, and bimanual conditions for Experiment 2. This is assured because these contrasts are orthogonal to the voxel-selection criterion, and the experimental design was fully balanced (Kriegeskorte et al. 2009). Also, any assessment of the correlation between left- and right-hand patterns can be made in an unbiased fashion, as the classification is performed independently for the 2 hands and selection is not biased toward specific patterns. For the decomposition analysis presented in Figure 7, we ensured through Monte-Carlo simulation that the selection criterion did not bias subsequent analyses.

Bottom Line: A second type of representation becomes evident in caudal premotor and anterior parietal cortices during bimanual actions.In these regions, ipsilateral actions are represented as nonlinear modulation of activity patterns related to contralateral actions, an encoding scheme that may provide the neural substrate for coordinating bimanual movements.We conclude that ipsilateral cortical representations change their informational content and functional role, depending on the behavioral context.

View Article: PubMed Central - PubMed

Affiliation: Institute of Cognitive Neuroscience, University College London, London, UK. j.diedrichsen@ucl.ac.uk

ABSTRACT
Movements of the upper limb are controlled mostly through the contralateral hemisphere. Although overall activity changes in the ipsilateral motor cortex have been reported, their functional significance remains unclear. Using human functional imaging, we analyzed neural finger representations by studying differences in fine-grained activation patterns for single isometric finger presses. We demonstrate that cortical motor areas encode ipsilateral movements in 2 fundamentally different ways. During unimanual ipsilateral finger presses, primary sensory and motor cortices show, underneath global suppression, finger-specific activity patterns that are nearly identical to those elicited by contralateral mirror-symmetric action. This component vanishes when both motor cortices are functionally engaged during bimanual actions. We suggest that the ipsilateral representation present during unimanual presses arises because otherwise functionally idle circuits are driven by input from the opposite hemisphere. A second type of representation becomes evident in caudal premotor and anterior parietal cortices during bimanual actions. In these regions, ipsilateral actions are represented as nonlinear modulation of activity patterns related to contralateral actions, an encoding scheme that may provide the neural substrate for coordinating bimanual movements. We conclude that ipsilateral cortical representations change their informational content and functional role, depending on the behavioral context.

Show MeSH
Related in: MedlinePlus