Hierarchically Organized Medial Frontal Cortex-Basal Ganglia Loops Selectively Control Task- and Response-Selection

Abstract

Adaptive behavior requires context-sensitive configuration of task-sets that specify time-varying stimulus-response mappings. Intriguingly, response time costs associated with changing task-sets and motor responses are known to be strongly interactive: switch costs at the task level are small in the presence of a response-switch but large when accompanied by a response-repetition, and vice versa for response-switch costs. The reasons behind this well known interdependence between task- and response-level control processes are currently not well understood. Here, we formalized and tested a model assuming a hierarchical organization of superordinate task-set and subordinate response-set selection processes to account for this effect. The model was found to successfully explain the full range of behavioral task- and response-switch costs across first and second order trial transitions. Using functional magnetic resonance imaging (fMRI) in healthy humans, we then characterized the neural circuitry mediating these effects. We found that presupplementary motor area (preSMA) activity tracked task-set control costs, SMA activity tracked response-set control costs, and basal ganglia (BG) activity mirrored the interaction between task- and response-set regulation processes that characterized participants' response times. A subsequent fMRI-guided transcranial magnetic stimulation experiment confirmed dissociable roles of the preSMA and SMA in determining response costs. Together, these data provide evidence for a hierarchical organization of posterior medial frontal cortex and its interaction with the BG, where a superordinate preSMA-BG loop establishes task-set selection, which imposes a (unidirectional) constraint on a subordinate SMA-BG loop that determines response-selection, resulting in the characteristic interdependence in task- and response-switch costs in behavior. The ability to use context-sensitive task-sets to guide our responses is central to human adaptive behavior. Task and response selection are strongly interactive: it is more difficult to repeat a response in the context of a changing task-set, and vice versa. However, the neurocognitive architecture giving rise to this interdependence is currently not understood. Here we use modeling, neuroimaging, and noninvasive neurostimulation to show that this phenomenon derives from a hierarchical organization of posterior medial frontal cortex and its interaction with the basal ganglia, where a more anterior corticostriatal loop establishes task-set selection, which constrains a more posterior loop responsible for response-selection. These data provide a neural explanation for a key behavioral signature of human cognitive control.

Uncovering hidden brain state dynamics that regulate performance and decision-making during cognition

“…Previous research has suggested an important role for this DMPFC region, which overlaps with the pre-supplementary motor areas, in both task control and action selection 58 . However, a recent study using an adaptive control task which required context-sensitive configuration of task-sets and stimulus–response mappings found that activation in the pre-SMA tracked task-set control cost but not response level control 59 . Intracranial recordings have further revealed that neuronal activity in the DMPFC is modulated by task-set but persistent activity in this region was not stimulus-specific 60 .…”

Motor Preparation Disrupts Proactive Control in the Stop Signal Task

“…In contrast, motor preparation engages predominantly left-hemispheric areas including the caudate head, AG and SFG as well as vmPFC and PCgC, core areas of the default model network (DMN). The pre-SMA is widely implicated in self control (Jaffard et al, 2008 ; Rushworth, 2008 ; Sharp et al, 2010 ; Cieslik et al, 2015 ; Hampshire and Sharp, 2015 ), and unlike the more posterior medial frontal structures that project to the lentiform nucleus, the pre-SMA projects to the caudate head (Zhang et al, 2012 ), in support of a hierarchical structure where anterior and posterior medial prefrontal regions each respond to task set and response control (Korb et al, 2017 ). As pre-SMA responds to conflict anticipation and the left caudate nucleus responds to motor preparation, it is likely that the right-hemispheric pre-SMA interacts with the left caudate head via its excitatory inputs to the right caudate head, which in turn inhibits the left caudate head through trans-hemispheric processes or subcortical mechanisms involving the pallidum (Watanabe et al, 2015 ).…”

Dynamic Trial-by-Trial Recoding of Task-Set Representations in the Frontoparietal Cortex Mediates Behavioral Flexibility

“…One major reason for this is that most functional magnetic resonance imaging (fMRI) studies delineating neural substrates of task switching have simply contrasted mean activity levels between switch and repeat cues or trials. This work has implicated the lateral inferior frontal cortex, the presupplementary motor area (pre-SMA), superior and inferior parietal cortices, and the striatum in switch processes (Dove et al, 2000;Sohn et al, 2000;Brass andvon Cramon, 2002, 2004;Johnston et al, 2007;Braem et al, 2013;Ruge et al, 2013;Korb et al, 2017). However, mean activation contrasts cannot speak directly to these regions' potential roles in representing and modifying task sets.…”