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Hand use predicts the structure of representations in sensorimotor cortex

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Abstract

Fine finger movements are controlled by the population activity of neurons in the hand area of primary motor cortex. Experiments using microstimulation and single-neuron electrophysiology suggest that this area represents coordinated multi-joint, rather than single-finger movements. However, the principle by which these representations are organized remains unclear. We analyzed activity patterns during individuated finger movements using functional magnetic resonance imaging (fMRI). Although the spatial layout of finger-specific activity patterns was variable across participants, the relative similarity between any pair of activity patterns was well preserved. This invariant organization was better explained by the correlation structure of everyday hand movements than by correlated muscle activity. This also generalized to an experiment using complex multi-finger movements. Finally, the organizational structure correlated with patterns of involuntary co-contracted finger movements for high-force presses. Together, our results suggest that hand use shapes the relative arrangement of finger-specific activity patterns in sensory-motor cortex.

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Figure 1: Evoked activity patterns during single finger presses of the left hand in the hand area of the right primary motor cortex, recorded from three different participants at 3T.
Figure 2: Pattern stability across a period of 6 months in a group of nine separate participants.
Figure 3: Representational structure of finger movements in M1.
Figure 4: Representational structure in M1 is best explained by natural statistics of hand use.
Figure 5: Alternative models for explaining single-finger distances.
Figure 6: Multi-finger configuration task.
Figure 7: Enslaving during single finger movements.

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Acknowledgements

We thank J. Ingram and D. Wolpert, as well as A. Faisal and A. Thomik, for sharing their natural statistics data sets, G. Prichard, S. Clare, J. O'Reilly for help with the acquisition of the 7T data set, and J. Xu, B. Hertler, M. Brentscheidt, M. Wilmer, A. Luft, P. Celnik and J. Krakauer for sharing the data regarding stability of finger representations. Finally we thank J. Krakauer, J. Xu, K. Longden and A. Saleem for helpful comments on the manuscript. The research was supported by grants by the Wellcome trust (094874/Z/10/Z) and James McDonnell foundation to J.D. The Wellcome Trust Centre for Neuroimaging is supported by core funding from the Wellcome Trust (091593/Z/10/Z).

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Authors and Affiliations

  1. Institute of Cognitive Neuroscience, University College London, London, UK

    Naveed Ejaz & Jörn Diedrichsen

  2. Department of Neurology, University of Tokyo, Tokyo, Japan

    Masashi Hamada

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  1. Naveed Ejaz
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  2. Masashi Hamada
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  3. Jörn Diedrichsen
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Contributions

N.E. and J.D. were jointly responsible for design of experiments, analysis and writing of the manuscript. N.E. contributed the data for the multi-finger experiment and M.H. was instrumental in the muscle activity recording.

Corresponding author

Correspondence to Jörn Diedrichsen.

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The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Evoked activity patterns during left-hand finger presses in right S1 of 3 exemplary participants.

The black line indicates the fundus of the central sulcus, while the white dashed lines show the boundaries between Brodmann areas (see inset) are estimated using a probabilistic surface-based cytoarchitectonic atlas (Fischl, B., et al. (2008) Cereb Cortex 18, 1973-1980).

Supplementary Figure 2 Individual anatomical and functional maps after spherical inter-subject normalisation driven solely by anatomical criteria

A ~5x5cm area around the hand knob is shown. The left hemispheres are flipped, such that posterior regions are to the left and anterior regions to the right. (a) Sulcal depth maps with sulci shown in dark and gyri in light shades. (b) Pattern distance averaged across all 10 possible digit pairs for the contralateral hand, estimated using a cortical searchlight analysis (Oosterhof, N.N. et al. (2011) Neuroimage 56, 593-600), indicates the location of the functional hand area in M1 and S1.

Supplementary Figure 3 Distance between activation patterns in somatosensory cortex

(a) Cross-validated Mahalanobis distance between patterns for all digits in right S1 for the three participants depicted in Figure 1. (b) Distances between activity patterns for digit 1-5 averaged over the 12 hemispheres. (c) Multi-dimensional scaling of the pattern distances in two-dimensional space. Ellipses show standard error of the mean after procrustes alignment across hemispheres. There were significant differences between distance structures in M1 and S1: After normalising the distances in each ROI by the mean distance, the distances 2-3, 2-4, and 3-4 were larger in S1 than in M1, while the distance 1-5 was larger in M1 than in S1 (all t11> 3.7, p<0.02 after Bonferroni-correction for multiple tests).

Supplementary Figure 4 Finger representation as revealed by high-resolution fMRI at 7T

(a) Evoked activity patterns during single finger movements of the right hand in the left primary motor cortex of one individual. The dotted line indicates the fundus of the central sulcus. (b) Multi-dimensional scaling of the pattern distances in S1 (c) and M1.

Supplementary Figure 5 Distance structures for hand usage estimated from two independent studies

In the Thomik and Faisal study, 8 right-handed participants performed everyday tasks. Joint kinematics data was recorded simultaneously for both hands and the distance structure for each hand was estimated in exactly the same way as reported previously for the Ingram et al. 2008 study.

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Ejaz, N., Hamada, M. & Diedrichsen, J. Hand use predicts the structure of representations in sensorimotor cortex. Nat Neurosci 18, 1034–1040 (2015). https://doi.org/10.1038/nn.4038

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