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Frontostriatal dynamics of cognitive control

Thomas W. ElstoniD, Joni D. WallisiD

Abstract

A central tenet of cognitive psychology is the existence of two distinct modes of processing: the fast, automatic system and the slow, deliberative system 1,2. The prefrontal cortex is thought to control the balance between these two systems, allowing automatic processing where possible, but stepping in when deliberative processes are required, such as in novel, uncertain, or conflicting situations 3-6. Despite the central importance of this idea in cognitive neuroscience, there is little understanding of how this control process is implemented. We used Neuropixel recordings in rhesus macaques to decode neural activity and reveal the cognitive processes in prefrontal cortex and striatum during automatic and deliberative decisions. During automatic decisions, the chosen option was decoded simultaneously from both areas. During deliberative choices, the prefrontal cortex serially considered multiple options while neither could be decoded from the striatum. This suppression occurred via an increase in alpha band coherence between the two structures and scaled with the volatility of prefrontal representations. Our findings reveal a specific neural mechanism that may explain how frontostriatal circuits implement cognitive control and provide a novel mechanism by which to treat disorders of behavioral control.

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