Abstract

A key aspect of behavioral inhibition is the ability to wait before acting. Failures in this form of inhibition result in impulsivity and are commonly observed in various neuropsychiatric disorders. Prior evidence has implicated medial frontal cortex, motor cortex, orbitofrontal cortex (OFC), and ventral striatum in various aspects of inhibition. Here, using distributed recordings of brain activity [with local-field potentials (LFPs)] in rodents, we identified oscillatory patterns of activity linked with action and inhibition. Low-frequency (δ) activity within motor and premotor circuits was observed in two distinct networks, the first involved in cued, sensory-based responses and the second more generally in both cued and delayed actions. By contrast, θ activity within prefrontal and premotor regions (medial frontal cortex, OFC, ventral striatum, and premotor cortex) was linked with inhibition. Connectivity at θ frequencies was observed within this network of brain regions. Interestingly, greater connectivity between primary motor cortex (M1) and other motor regions was linked with greater impulsivity, whereas greater connectivity between M1 and inhibitory brain regions (OFC, ventral striatum) was linked with improved inhibition and diminished impulsivity. We observed similar patterns of activity on a parallel task in humans: low-frequency activity in sensorimotor cortex linked with action, θ activity in OFC/ventral prefrontal cortex (PFC) linked with inhibition. Thus, we show that δ and θ oscillations form distinct large-scale networks associated with action and inhibition, respectively.

Highlights

  • Impulsivity has been recognized as a key dimension of behavior that co-occurs with various neuropsychiatric disorders

  • Using multisite local-field potential (LFP) recordings, we have identified large-scale brain networks involved in action and inhibition in segregated brain regions

  • While pharmacologic agents can ameliorate some forms of impulsivity (Moeller et al, 2001), a better understanding of the underlying brain systems associated with impulsivity is a key first step toward developing treatments targeted at this particular dimension of Author contributions: L.F., M.F., S.H., N.B., C.C., J.M., and D.S.R. designed research; L.F., M.F., P.B., T.T., S.H., N.B., C.C., A.T., A.G., J.M., and D.S.R. performed research; L.F., M.F., P.B., T.T., H.X., Z.X., J.M., and D.S.R. analyzed data; M.F., P.B., J.M.M., and D.S.R. wrote the paper

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Summary

Introduction

Impulsivity has been recognized as a key dimension of behavior that co-occurs with various neuropsychiatric disorders (such as bipolar disorder, ADHD, and brain injury; Moeller et al, 2001). While pharmacologic agents can ameliorate some forms of impulsivity (Moeller et al, 2001), a better understanding of the underlying brain systems associated with impulsivity is a key first step toward developing treatments targeted at this particular dimension of Author contributions: L.F., M.F., S.H., N.B., C.C., J.M., and D.S.R. designed research; L.F., M.F., P.B., T.T., S.H., N.B., C.C., A.T., A.G., J.M., and D.S.R. performed research; L.F., M.F., P.B., T.T., H.X., Z.X., J.M., and D.S.R. analyzed data; M.F., P.B., J.M.M., and D.S.R. wrote the paper. Research Article: New Research 2 of 20 psychopathology (Dalley and Robbins, 2017). Progress has been made through the careful development of behavioral tasks that measure specific aspects of behavioral inhibition and impulsivity

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