Abstract

Flexible behavior requires restraint of actions that are no longer appropriate. This behavioral inhibition critically relies on frontal cortex - basal ganglia circuits. Within the basal ganglia, the globus pallidus pars externa (GPe) has been hypothesized to mediate selective proactive inhibition: being prepared to stop a specific action, if needed. Here we investigate population dynamics of rat GPe neurons during preparation-to-stop, stopping, and going. Rats selectively engaged proactive inhibition towards specific actions, as shown by slowed reaction times (RTs). Under proactive inhibition, GPe population activity occupied state-space locations farther from the trajectory followed during normal movement initiation. Furthermore, the state-space locations were predictive of distinct types of errors: failures-to-stop, failures-to-go, and incorrect choices. Slowed RTs on correct proactive trials reflected starting bias towards the alternative action, which was overcome before progressing towards action initiation. Our results demonstrate that rats can exert cognitive control via strategic adjustments to their GPe network state.

Highlights

  • Our capacity for self-restraint is critical for adaptive behavior

  • On some trials the Go cue was quickly followed by a Stop cue, indicating that the rat instead needed to maintain its nose in the starting hole to trigger reward delivery

  • Stop-signal tasks are widely-used to test cognitive control (Lipszyc and Schachar, 2010), with proactive inhibition considered especially reliant on top-down, effortful, resource-demanding processes (Jahanshahi et al, 2015)

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Summary

Introduction

Our capacity for self-restraint is critical for adaptive behavior. Dysfunctions in behavioral inhibition are involved in many human disorders, including drug addiction (Ersche et al, 2012). ‘Reactive’ inhibition – making quick use of a Stop cue – appears to involve at least two distinct mechanisms (Schmidt and Berke, 2017): a rapid Pause process mediated via the subthalamic nucleus (STN; Aron and Poldrack, 2006; Schmidt et al, 2013) followed by a Cancel process achieved through pallidostriatal inhibition (Mallet et al, 2016). Behavioral inhibition can be ‘proactive’: restraint of actions, in advance of any Stop cue. A key behavioral signature of proactive inhibition is slowing of reaction times (RTs) for that action, when the anticipated Stop cue does not occur In some studies, fitting of models to behavioral data has suggested that slowed RTs reflect raising of a

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