Cortical-subcortical interactions in goal-directed behavior

Abstract

Flexibly selecting appropriate actions in response to complex, ever-changing environments requires both cortical and subcortical regions, which are typically described as participating in a strict hierarchy. In this traditional view, highly specialized subcortical circuits allow for efficient responses to salient stimuli, at the cost of adaptability and context-specificity, which are attributed to the neocortex. Their interactions are often described as the cortex providing top-down command signals for subcortical structures to implement; however, as available technologies develop, studies increasingly demonstrate that behavior is represented by brain-wide activity and that even subcortical structures contain early signals of choice, suggesting that behavioral functions emerge as a result of different regions interacting as truly collaborative networks. In this review, we discuss the field's evolving understanding of how cortical and subcortical regions in placental mammals interact cooperatively- not only via top-down cortical-subcortical inputs, but through bottom-up interactions, especially via the thalamus. We describe our current understanding of the circuitry of both the cortex and two exemplar subcortical structures- the superior colliculus and striatum- to identify which information is prioritized by which regions. We then describe the functional circuits these regions form with one another- and the thalamus- to create parallel loops and complex networks for brain-wide information flow. Finally, we challenge the classic view that functional modules are contained within specific brain regions; instead, we propose that certain regions prioritize specific types of information over others, but the subnetworks they form- defined by their anatomical connections and functional dynamics- are the basis of true specialization.

Reduced recruitment of inhibitory control regions in very young children with ADHD during a modified Kiddie Continuous Performance Task: a fMRI study

“…In models of inhibitory control, pre-SMA and striatum (including caudate) play a role in the downstream selection of a competing action among a space of possible action programs. The dorsal striatum is uniquely situated as the inter-face between cortex and the rest of the basal ganglia, forming part of an indirect cortico-basal ganglia-thalamic loop involved in action selection [100]. In a study of adults with ADHD, Sebastian and colleagues [105] found less activation in right caudate for people with ADHD compared to control participants, which is in line with what we report here.…”

“…In addition to the lateral cortical regions, we also observed group differences in the bilateral caudate and medial frontal cortical regions, including the anterior cingulate and pre-SMA. These regions are crucial nodes in the neural system involved in stopping behaviors, such as the ability to withhold a response in the K-CPT [100, 85, 101, 102, 103, 96, 104]. In models of inhibitory control, pre-SMA and striatum (including caudate) play a role in the downstream selection of a competing action among a space of possible action programs.…”

“…In addition to the lateral cortical regions, we also observed group differences in the bilateral caudate and medial frontal cortical regions, including the anterior cingulate and pre-SMA. These regions are crucial nodes in the neural system involved in stopping behaviors, such as the ability to withhold a response in the K-CPT [100,85,101,102,103,96,104].…”

Data-based large-scale models provide a window into the organization of cortical computations

“…But this needs to be done in a way that still supports fast simulations of large-scale models, so that training of these models for specific computational tasks remains computationally feasible. In addition, the computational role of projections to and synaptic inputs from subcortical areas, such as basal ganglia and the thalamus (see [Cruz et al, 2023] for a recent review), needs to be modeled and analyzed through integrated large-scale models. Altogether, this work is likely to complement, challenge, and enhance experimental work in vivo that aims at clarifying the organization of brain computations.…”

Motor cortex is required for flexible but not automatic motor sequences

“…3). These results suggest that motor cortex funnels information from behaviorally-relevant cortical computations -e.g., about environmental events or working memory processes -to subcortical motor circuits, making them integral to executing complex flexible behaviors 11,18,20,25,63,64 . From an evolutionary perspective this makes sense: rather than duplicating or reinventing the robust and effective control functions of subcortical systems, motor cortex can provide an adaptive advantage by orchestrating downstream controllers based on information uniquely available to it.…”