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Canceling actions involves a race between basal ganglia pathways

Nature Neuroscience volume 16, pages 11181124 (2013) | Download Citation

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Abstract

Salient cues can prompt the rapid interruption of planned actions. It has been proposed that fast, reactive behavioral inhibition involves specific basal ganglia pathways, and we tested this by comparing activity in multiple rat basal ganglia structures during performance of a stop-signal task. Subthalamic nucleus (STN) neurons exhibited low-latency responses to 'Stop' cues, irrespective of whether actions were canceled or not. By contrast, neurons downstream in the substantia nigra pars reticulata (SNr) only responded to Stop cues in trials with successful cancellation. Recordings and simulations together indicate that this sensorimotor gating arises from the relative timing of two distinct inputs to neurons in the SNr dorsolateral 'core' subregion: cue-related excitation from STN and movement-related inhibition from striatum. Our results support race models of action cancellation, with stopping requiring Stop-cue information to be transmitted from STN to SNr before increased striatal input creates a point of no return.

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Acknowledgements

We thank V. Stuphorn, D. Weissman, A. Aron, G. Morris, M. Churchland, M. Bevan and D. Meyer for their helpful comments. J. Pettibone and A. Case provided valuable assistance. This work was supported by Deutsche Forschungsgemeinschaft grant SCHM 2745/1-1, the US National Institute on Drug Abuse, National Institute on Neurological Disorders and Stroke, and the University of Michigan.

Author information

Affiliations

  1. Department of Psychology, University of Michigan, Ann Arbor, Michigan, USA.

    • Robert Schmidt
    • , Nicolas Mallet
    • , Fujun Chen
    •  & Joshua D Berke
  2. Department of Neurology, University of Michigan, Ann Arbor, Michigan, USA.

    • Daniel K Leventhal
  3. Centre National de la Recherche Scientifique, Institut des Maladies Neurodégénératives, Université Victor-Segalen, Bordeaux, France.

    • Nicolas Mallet

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Contributions

J.D.B. designed and oversaw the project. D.K.L. helped develop the behavioral task. D.K.L., N.M. and F.C. performed electrophysiological experiments. R.S. developed and performed the data analyses and computational modeling. R.S. and J.D.B. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Joshua D Berke.

Supplementary information

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    Supplementary Figures and Text

    Supplementary Figures 1–10 and Supplementary Table 1

Videos

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    Supplementary Video 1

    Video recording of a rat performing Go and Stop trials

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DOI

https://doi.org/10.1038/nn.3456

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