Frontosubthalamic Circuits for Control of Action and Cognition

Abstract

The subthalamic nucleus (STN) of the basal ganglia appears to have a potent role in action and cognition. Anatomical and imaging studies show that different frontal cortical areas directly project to the STN via so-called hyperdirect pathways. This review reports some of the latest findings about such circuits, including simultaneous recordings from cortex and the STN in humans, single-unit recordings in humans, high-resolution fMRI, and neurocomputational modeling. We argue that a major function of the STN is to broadly pause behavior and cognition when stop signals, conflict signals, or surprise signals occur, and that the fronto-STN circuits for doing this, at least for stopping and conflict, are dissociable anatomically and in terms of their spectral reactivity. We also highlight recent evidence for synchronization of oscillations between prefrontal cortex and the STN, which may provide a preferential "window in time" for single neuron communication via long-range connections.

Keywords: basal ganglia; conflict; oscillations; response inhibition; stopping; surprise.

Figure 1.

Hypothetical model of different hyperdirect cortico-STN pathways for stopping and conflict processing. A, Stopping is initiated via right inferior frontal gyrus (R-IFG) (possibly in concert with pre-SMA), which projects to the central part of the STN. The STN topography in the figure is based on monkey tracing, with areas color coded by cortical inputs (orange represents ventromedial frontal; region not shown) (Haynes and Haber, 2013). There is a putatively broad effect on the GPi, which broadly suppresses thalamocortical drive, ultimately affecting primary motor and premotor representations. Increases in beta band power are prominent. B, Conflict operates in an analogous way, except it appears to be generated by dmPFC (perhaps pre-SMA), and this projects to a somewhat more dorsal STN territory. Power increases now occur for low-frequency oscillations, LFOs, in the 2–8 Hz band.