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The Journal of Neuroscience, October 14, 2009, 29(41):12948-12956; doi:10.1523/JNEUROSCI.2471-09.2009

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Behavioral/Systems/Cognitive
Cortical Representation of Ipsilateral Arm Movements in Monkey and Man

Karunesh Ganguly,^1,2,6 * Lavi Secundo,^2 * Gireeja Ranade,¹ Amy Orsborn,³ Edward F. Chang,⁷ Dragan F. Dimitrov,⁷ Jonathan D. Wallis,^2,4 Nicholas M. Barbaro,⁷ Robert T. Knight,^2,4,6,7 and Jose M. Carmena^1,2,3,5

¹Department of Electrical Engineering and Computer Sciences, ²Helen Wills Neuroscience Institute, ³University of California San Francisco/University of California Berkeley Joint Graduate Group in Bioengineering, ⁴Department of Psychology, and ⁵Program in Cognitive Science, University of California Berkeley, Berkeley, California 94720, and ⁶Departments of Neurology and ⁷Neurosurgery, University of California San Francisco, San Francisco, California 94143

Correspondence should be addressed to Jose M. Carmena, 754 Sutardja Dai Hall, Berkeley, CA 94720-1770. Email: carmena{at}eecs.berkeley.edu

A fundamental organizational principle of the primate motor system is cortical control of contralateral limb movements. Motor areas also appear to play a role in the control of ipsilateral limb movements. Several studies in monkeys have shown that individual neurons in primary motor cortex (M1) may represent, on average, the direction of movements of the ipsilateral arm. Given the increasing body of evidence demonstrating that neural ensembles can reliably represent information with a high temporal resolution, here we characterize the distributed neural representation of ipsilateral upper limb kinematics in both monkey and man. In two macaque monkeys trained to perform center-out reaching movements, we found that the ensemble spiking activity in M1 could continuously represent ipsilateral limb position. Interestingly, this representation was more correlated with joint angles than hand position. Using bilateral electromyography recordings, we excluded the possibility that postural or mirror movements could exclusively account for these findings. In addition, linear methods could decode limb position from cortical field potentials in both monkeys. We also found that M1 spiking activity could control a biomimetic brain–machine interface reflecting ipsilateral kinematics. Finally, we recorded cortical field potentials from three human subjects and also consistently found evidence of a neural representation for ipsilateral movement parameters. Together, our results demonstrate the presence of a high-fidelity neural representation for ipsilateral movement and illustrates that it can be successfully incorporated into a brain–machine interface.

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Received May 27, 2009; revised Aug. 30, 2009; accepted Sept. 2, 2009.

Correspondence should be addressed to Jose M. Carmena, 754 Sutardja Dai Hall, Berkeley, CA 94720-1770. Email: carmena{at}eecs.berkeley.edu

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