Frontal circuit specialisations for decision making

Abstract

There is widespread consensus that distributed circuits across prefrontal and anterior cingulate cortex (PFC/ACC) are critical for reward‐based decision making. The circuit specialisations of these areas in primates were likely shaped by their foraging niche, in which decision making is typically sequential, attention‐guided and temporally extended. Here, I argue that in humans and other primates, PFC/ACC circuits are functionally specialised in two ways. First, microcircuits found across PFC/ACC are highly recurrent in nature and have synaptic properties that support persistent activity across temporally extended cognitive tasks. These properties provide the basis of a computational account of time‐varying neural activity within PFC/ACC as a decision is being made. Second, the macrocircuit connections (to other brain areas) differ between distinct PFC/ACC cytoarchitectonic subregions. This variation in macrocircuit connections explains why PFC/ACC subregions make unique contributions to reward‐based decision tasks and how these contributions are shaped by attention. They predict dissociable neural representations to emerge in orbitofrontal, anterior cingulate and dorsolateral prefrontal cortex during sequential attention‐guided choice, as recently confirmed in neurophysiological recordings.

Filling the gaps: Cognitive control as a critical lens for understanding mechanisms of value-based decision-making

“…These findings are consistent with an emerging new perspective that frames decision-making as a process of active information search rather than simply the passive accumulation of reward estimates (Hunt, 2021). This view not only bridges decision-making with active informationsampling (Boldt, Blundell, & De Martino, 2019;Cohen, McClure, & Yu, 2007;Gottlieb, 2018;Gottlieb, Cohanpour, Li, Singletary, & Zabeh, 2020;Gottlieb & Oudeyer, 2018;Hunt et al, 2018;Hunt, Rutledge, Malalasekera, Kennerley, & Dolan, 2016;Kaanders, Nili, O'Reilly, & Hunt, 2020), extended behaviors (Callaway, van Opheusden, et al, 2021;Holroyd & Yeung, 2012), and learning (Behrens, Woolrich, Walton, & Rushworth, 2007;Frömer et al, 2020;Nassar et al, 2012;O'Reilly, 2013), it also renders decision-making fundamentally a control problem.…”

Neural Representation of Costs and Rewards in Decision Making

“…It used to be believed that midbrain dopaminergic neurons (ventral segmental area, VTA) encode reward quantitatively in their phasic firing rate [34,35]. Interestingly, these neurons also encode the probability of acquiring the future reward [14], but they still fail to differentiate the motivational cue from subjective value perception. Fiorillo and his team [36] have shown that the existence of a dopamine ramp in the VTA dopaminergic neurons during the time between the perception of conditioned stimuli and the delivery of an actual reward when the stimuli predicted that the probability of the future reward was between 0 and 1.0.…”

“…The orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC) have long been shown to have activities that are correlated with task value and that are closely involved in decision making [OFC: 21,22; ACC: 23,24]. However, the differences between these two regions are revealed by their macrocircuit: OFC shows strong connections to areas in the ventral visual stream and the temporal lobe, which contain highly processed sensory information; ACC, however, shows strong connections to the dorsal striatum (putamen and caudate) and supplementary motor areas [14]. This means that the OFC possibly converges the multimodal sensory information for reward prediction, while the ACC may guide action selection to obtain rewards.…”

“…Various studies show how different brain areas are involved in the decision-making process, but few discuss the molecular mechanism behind it. Recently, Hunt [14] suggested the frontal microcircuits in the prefrontal cortex and the anterior cingulate cortex (PFC/ACC) may support temporary extended cognitive decision. The microcircuits in the PFC/ACC are recurrent in nature and can sustain their activities over time through NMDA receptor-mediated effects that have a longer decay time constant [14].…”

“…When it comes to deciding what the ultimate choice might be, these brain regions do not work in isolation. A decision is made through an interconnected, distributed, recurrent network with an emergent property [14,15], and choices are weighted by internal states at the nucleus accumbens before action selection [16].…”