Neural Mechanisms of Human Decision-Making.

We present a theory and neural network model of the neural mechanisms underlying human decision-making. We propose a detailed model of the interaction between brain regions, under a proposer-predictor-actor-critic​ ​framework. This theory is based on detailed animal data and theories of action-selection. Those theories are adapted to serial operation to bridge levels of analysis and explain human decision-making. Task-relevant areas of cortex propose a candidate plan using fast, model-free, parallel neural computations. Other areas of cortex and medial temporal lobe can then predict​ likely outcomes of that plan in this situation. This optional prediction- (or model-) based computation can produce better accuracy and generalization, at the expense of speed. Next, linked regions of basal ganglia act​ to accept or reject the proposed plan based on its reward history in similar contexts. If that plan is rejected, the process repeats to consider a new option. The reward-prediction system acts as a critic​ to determine the value of the outcome relative to expectations and produce dopamine as a training signal for cortex and basal ganglia. By operating sequentially and hierarchically, the same mechanisms previously proposed for animal action-selection could explain the most complex human plans and decisions. We discuss explanations of model-based decisions, habitization, and risky behavior based on the computational model.

A systems-neuroscience model of phasic dopamine.

We describe a neurobiologically informed computational model of phasic dopamine signaling to account for a wide range of findings, including many considered inconsistent with the simple reward prediction error (RPE) formalism. The central feature of this PVLV framework is a distinction between a primary value (PV) system for anticipating primary rewards (Unconditioned Stimuli [USs]), and a learned value (LV) system for learning about stimuli associated with such rewards (CSs). The LV system represents the amygdala, which drives phasic bursting in midbrain dopamine areas, while the PV system represents the ventral striatum, which drives shunting inhibition of dopamine for expected USs (via direct inhibitory projections) and phasic pausing for expected USs (via the lateral habenula). Our model accounts for data supporting the separability of these systems, including individual differences in CS-based (sign-tracking) versus US-based learning (goal-tracking). Both systems use competing opponent-processing pathways representing evidence for and against specific USs, which can explain data dissociating the processes involved in acquisition versus extinction conditioning. Further, opponent processing proved critical in accounting for the full range of conditioned inhibition phenomena, and the closely related paradigm of second-order conditioning. Finally, we show how additional separable pathways representing aversive USs, largely mirroring those for appetitive USs, also have important differences from the positive valence case, allowing the model to account for several important phenomena in aversive conditioning. Overall, accounting for all of these phenomena strongly constrains the model, thus providing a well-validated framework for understanding phasic dopamine signaling. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

How Sequential Interactive Processing Within Frontostriatal Loops Supports a Continuum of Habitual to Controlled Processing.

We address the distinction between habitual/automatic vs. goal-directed/controlled behavior, from the perspective of a computational model of the frontostriatal loops. The model exhibits a continuum of behavior between these poles, as a function of the interactive dynamics among different functionally-specialized brain areas, operating iteratively over multiple sequential steps, and having multiple nested loops of similar decision making circuits. This framework blurs the lines between these traditional distinctions in many ways. For example, although habitual actions have traditionally been considered purely automatic, the outer loop must first decide to allow such habitual actions to proceed. Furthermore, because the part of the brain that generates proposed action plans is common across habitual and controlled/goal-directed behavior, the key differences are instead in how many iterations of sequential decision-making are taken, and to what extent various forms of predictive (model-based) processes are engaged. At the core of every iterative step in our model, the basal ganglia provides a "model-free" dopamine-trained Go/NoGo evaluation of the entire distributed plan/goal/evaluation/prediction state. This evaluation serves as the fulcrum of serializing otherwise parallel neural processing. Goal-based inputs to the nominally model-free basal ganglia system are among several ways in which the popular model-based vs. model-free framework may not capture the most behaviorally and neurally relevant distinctions in this area.