Abstract
Devaluation is the key experimental paradigm used to demonstrate the presence of instrumental behaviors guided by goals in mammals. We propose a neural system-level computational model to address the question of which brain mechanisms allow the current value of rewards to control instrumental actions. The model pivots on and shows the computational soundness of the hypothesis for which the internal representation of instrumental manipulanda (e.g., levers) activate the representation of rewards (or “action-outcomes”, e.g., foods) while attributing to them a value which depends on the current internal state of the animal (e.g., satiation for some but not all foods). The model also proposes an initial hypothesis of the integrated system of key brain components supporting this process and allowing the recalled outcomes to bias action selection: (a) the sub-system formed by the basolateral amygdala and insular cortex acquiring the manipulanda-outcomes associations and attributing the current value to the outcomes; (b) three basal ganglia-cortical loops selecting respectively goals, associative sensory representations, and actions; (c) the cortico-cortical and striato-nigro-striatal neural pathways supporting the selection, and selection learning, of actions based on habits and goals. The model reproduces and explains the results of several devaluation experiments carried out with control rats and rats with pre- and post-training lesions of the basolateral amygdala, the nucleus accumbens core, the prelimbic cortex, and the dorso-medial striatum. The results support the soundness of the hypotheses of the model and show its capacity to integrate, at the system-level, the operations of the key brain structures underlying devaluation. Based on its hypotheses and predictions, the model also represents an operational framework to support the design and analysis of new experiments on the motivational aspects of goal-directed behavior.
Highlights
The capacity to select actions on the basis of desired goals is a fundamental evolutionary acquisition of animals’ adaptive flexibility
Notwithstanding the large number of experiments on instrumental devaluation effects (IDE), there are still few works proposing comprehensive system-level accounts of the neural basis of IDE and its role in goal-directed behavior. These works have an important theoretical value but do not achieve the operational detail of computational models. We address this problem and in particular we focus on two key questions: (a) how does an animal recall the motivational value of outcomes in IDE experiments? (b) how does this value support the selection of goals? We start to address the question: what is the brain system through which the selection of goals translates into the selection of suitable actions to pursue them? These questions are important as they are at the core of our understanding of goal-directed behavior, in turn playing a central role for animals endowed with flexible cognition (Balleine and Dickinson, 1998; Mannella et al, 2013)
The main hypothesis of the model is that (a) the evaluation processes of the rewards involving IDE are based on the associations between the representations of external stimuli involved in the instrumental conditioning, in particular the manipulanda, and the representations of action outcomes, in particular the rewarding foods, and that (b) the value attributed to such outcomes depends on the current state of the animal
Summary
The capacity to select actions on the basis of desired goals (goal-directed behavior) is a fundamental evolutionary acquisition of animals’ adaptive flexibility. The model incorporates and operationalizes additional hypotheses related to how the selected goal leads to bias the selection of actions to perform: (a) the brain system underlying IDE and goal-directed behavior is based on three basal gangliacortical (BG-Ctx) loops involving ventral basal ganglia-PFC (BGv-PFC; “limbic loop,” called here “goal loop” for the focus on goal-directed behavior), dorsomedial BG-posterior parietal cortex (BGdm-PPC; “associative loop”), and dorsolateral BGmotor cortex (BGdl-MC; “motor loop”) (Yin and Knowlton, 2006; Baldassarre et al, 2013b; Fiore et al, 2014); (b) goals are stored and selected within the goal loop (Passingham and Wise, 2012), in particular involving NAc and PL, and value information is conveyed to it from BLA/IC through NAc (Mannella et al, 2013); (c) learning processes involving the BLA/IC-NAc-PL axis are guided by cortico-cortical pathways encompassing MC, PPC, and PFC, and encoding actionoutcome associations (Mannella and Baldassarre, 2015); (d) goals selected by the goal loop bias action selection processes via goal-action associations encoded in both sub-cortical pathways (involving dopaminergic spirals and dorsomedial striatum— DMS; Belin et al, 2009) and cortico-cortical pathways (involving PL, PPC, and MC; Caligiore et al, 2010; Baldassarre et al, 2013a) These hypotheses derive from: (a) empirical evidence concerning the brain structures involved in IDE; (b) general neuroscientific knowledge related to such brain structures; (c) the cited modeling/theoretical works; (d) the computational constraints generated by the model during its construction and test.
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