Abstract
Coordinated spiking activity in neuronal ensembles, in local networks and across multiple cortical areas, is thought to provide the neural basis for cognition and adaptive behavior. Examining such collective dynamics at the level of single neuron spikes has remained, however, a considerable challenge. We found that the spiking history of small and randomly sampled ensembles (∼20−200 neurons) could predict subsequent single neuron spiking with substantial accuracy in the sensorimotor cortex of humans and nonhuman behaving primates. Furthermore, spiking was better predicted by the ensemble's history than by the ensemble's instantaneous state (Ising models), emphasizing the role of temporal dynamics leading to spiking. Notably, spiking could be predicted not only by local ensemble spiking histories, but also by spiking histories in different cortical areas. These strong collective dynamics may provide a basis for understanding cognition and adaptive behavior at the level of coordinated spiking in cortical networks.
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Acknowledgements
We thank M.R. Fellows, C. Vargas-Irwin and B. Philip for collecting the nonhuman primate data. We thank our clinical trial participants for their dedication to this research, G. Friehs for his role as surgical investigator for the pilot clinical trial, J. Mukand for his role as clinical investigator for the pilot clinical trial, and A. Caplan, M. Serruya, M. Saleh and other employees of Cyberkinetics Neurotechnology Systems for data collection, manufacturing and clinical trial management. This study was based on work supported in part by the Office of Research and Development, Rehabilitation R&D Service, Department of Veterans Affairs (L.R.H. and J.P.D.). This work was supported by the National Institute of Neurological Disorders and Stroke (5K01NS057389-02 to W.T. and NS-25074 (Javits Award) to J.P.D.), the National Institute of Child Health and Human Development/National Center for Medical Rehabilitation Research (N01-HD-53403, subcontract to L.R.H.), the Massachusetts General Hospital Deane Institute (L.R.H.), the Doris Duke Charitable Foundation (L.R.H) and the National Institute on Deafness and Other Communication Disorders (R01-DC-009899 to L.R.H.).
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W.T. conceived the study's central ideas and conducted the data analyses. W.T. wrote the paper with contributions from L.R.H. and J.P.D. L.R.H. and J.P.D. contributed to the clinical research design. L.R.H. was the principal investigator for the pilot clinical trial. J.P.D. supervised the nonhuman primate experiments.
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J.P.D. was Chief Scientific Officer, director, and received stock holdings and compensation from Cyberkinetics Neurotechnology Systems. L.R.H. received research support from Massachusetts General and Spaulding Rehabilitation Hospitals, which in turn received clinical trial support from Cyberkinetics Neurotechnology Systems, which ceased operation in 2009. The BrainGate pilot clinical trials are now directed by Massachusetts General Hospital.
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Truccolo, W., Hochberg, L. & Donoghue, J. Collective dynamics in human and monkey sensorimotor cortex: predicting single neuron spikes. Nat Neurosci 13, 105–111 (2010). https://doi.org/10.1038/nn.2455
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DOI: https://doi.org/10.1038/nn.2455
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