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Canceling actions involves a race between basal ganglia pathways

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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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Figure 1: Task events and behavior.
Figure 2: Distinct processing of the Stop cue across basal ganglia components.
Figure 3: Stop cues increase firing in STN before SNr.
Figure 4: An SNr hotspot for Stop cue responses.
Figure 5: Variable timing of a striatal go process critically determines whether stopping is successful.
Figure 6: Modeling sensorimotor gating in SNr neurons.

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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.

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Authors

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.

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Correspondence to Joshua D Berke.

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The authors declare no competing financial interests.

Supplementary information

Supplementary Figures and Text

Supplementary Figures 1–10 and Supplementary Table 1 (PDF 14373 kb)

Supplementary Video 1

Video recording of a rat performing Go and Stop trials (MOV 3332 kb)

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Schmidt, R., Leventhal, D., Mallet, N. et al. Canceling actions involves a race between basal ganglia pathways. Nat Neurosci 16, 1118–1124 (2013). https://doi.org/10.1038/nn.3456

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