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Neural cognitive signals during spontaneous movements in the macaque

Nature Neuroscience volume 26, pages 295–305 (2023)Cite this article

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Abstract

The single-neuron basis of cognitive processing in primates has mostly been studied in laboratory settings where movements are severely restricted. It is unclear, therefore, how natural movements might affect neural signatures of cognition in the brain. Moreover, studies in mice indicate that body movements, when measured, account for most of the neural dynamics in the cortex. To examine these issues, we recorded from single-neuron ensembles in the prefrontal cortex in moving monkeys performing a cognitive task and characterized eye, head and body movements using video tracking. Despite considerable trial-to-trial movement variability, single-neuron tuning could be precisely measured and decision signals accurately decoded on a single-trial basis. Creating or abolishing spontaneous movements through head restraint and task manipulations had no measurable impact on neural responses. However, encoding models showed that uninstructed movements explained as much neural variance as task variables, with most movements aligned to task events. These results demonstrate that cognitive signals in the cortex are robust to natural movements, but also that unmeasured movements are potential confounds in cognitive neurophysiology experiments.

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Fig. 1: Task design and neural implants.
Fig. 2: Behavioral performance and movement tracking.
Fig. 3: Single-neuron and population analyses.
Fig. 4: Single-neuron and population analyses.
Fig. 5: Decoding analyses from neural ensembles.
Fig. 6: Manipulation of uninstructed movements through modified tasks.
Fig. 7: Modified tasks have no effect on neural population tuning.
Fig. 8: Neural encoding of task, instructed and uninstructed movements.

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Data availability

The data from this study will be stored on a public repository maintained by the Open Science Framework. The repository can be found at https://osf.io/zeqbp/.

Code availability

The MATLAB code used for the data analysis in this study is available online at https://osf.io/zeqbp/.

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Acknowledgements

We thank S. Musall, M. T. Kaufman and A. K. Churchland in providing assistance to replicate the methodology used in Musall et al.20. Financial support was received from the Canadian Institutes of Health Research Fellowship Award (S.T.), the Human Frontier Science Program (S.T.), the National Institutes of Health (5R01DC017690-02, R.W.D.) and a Natural Sciences and Engineering Research Council of Canada grant (M.P.).

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Author notes

  1. Sébastien Tremblay & Camille Testard

    Present address: Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA

  2. Jeanne Inchauspé

    Present address: Radcliffe Department of Medicine, University of Oxford, Oxford, UK

  3. These authors contributed equally: Sébastien Tremblay, Camille Testard.

Authors and Affiliations

  1. Montreal Neurological Institute, McGill University, Montreal, Quebec, Canada

    Sébastien Tremblay, Camille Testard, Jeanne Inchauspé & Michael Petrides

  2. Department of Neuroscience, University of Pennsylvania, Philadelphia, PA, USA

    Ron W. DiTullio

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Contributions

S.T., C.T. and M.P. designed the experiments. S.T., C.T. and J.I. trained the animals and recorded the data. S.T., C.T. and R.W.D. analyzed the data. S.T., C.T. and M.P. wrote the article with assistance from J.I. and R.W.D.

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Correspondence to Sébastien Tremblay.

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Nature Neuroscience thanks Simon Musall and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Tremblay, S., Testard, C., DiTullio, R.W. et al. Neural cognitive signals during spontaneous movements in the macaque. Nat Neurosci 26, 295–305 (2023). https://doi.org/10.1038/s41593-022-01220-4

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