Abstract
SummaryImpaired detection of causal relationships between actions and their outcomes can lead to maladaptive behavior. However, causal roles of specific prefrontal cortex (PFC) sub-regions and the caudate nucleus in mediating such relationships in primates are unclear. We inactivated and overactivated five PFC sub-regions, reversibly and pharmacologically: areas 24 (perigenual anterior cingulate cortex), 32 (medial PFC), 11 (anterior orbitofrontal cortex, OFC), 14 (rostral ventromedial PFC/medial OFC), and 14-25 (caudal ventromedial PFC) and the anteromedial caudate to examine their role in expressing learned action-outcome contingencies using a contingency degradation paradigm in marmoset monkeys. Area 24 or caudate inactivation impaired the response to contingency change, while area 11 inactivation enhanced it, and inactivation of areas 14, 32, or 14-25 had no effect. Overactivation of areas 11 and 24 impaired this response. These findings demonstrate the distinct roles of PFC sub-regions in goal-directed behavior and illuminate the candidate neurobehavioral substrates of psychiatric disorders, including obsessive-compulsive disorder.
Highlights
In everyday life, we continually make decisions based on our goals or go on ‘‘autopilot’’ to get through the day
We examined the contribution of five prefrontal and cingulate sub-regions: areas 32, 24, the boundary between areas 14 and 25, 11, and 14 using temporary pharmacological inactivation via local microinfusion of a combination of a GABAA agonist and a GABAB agonist
The marmosets were considered to behave in a goal-directed manner if they reduced their responding following the degradation of one of the A-O associations compared with when it was not degraded. Marmosets only altered their responding when the A-O associations were degraded when compared with sessions in which there were no free rewards (Figure 1D). These results indicated that the reduction in responding was not due to the presence of free rewards, but because of the weakening of perceived causality between a specific action and outcome
Summary
We continually make decisions based on our goals or go on ‘‘autopilot’’ to get through the day. Normal behaviors can either be goal directed, when performing an action to obtain a specific goal, or habitual, when a stimulus can trigger a well-learned response, regardless of its consequences. The goal-directed system is needed to adapt and remain flexible to changing environments and goals, whereas the habit system reduces cognitive load. Problems in the coordination and competition between the goal-directed and habitual systems are seen both in health (Balleine and O’Doherty, 2010; de Wit and Dickinson, 2009; Dolan and Dayan, 2013; Verhoeven and de Wit, 2018) and in neuropsychiatric disorders such as obsessivecompulsive disorder (OCD) (Gillan and Robbins, 2014; Robbins et al, 2019) and addiction (Ersche et al, 2016; Everitt and Robbins, 2005). Understanding the neurobiological basis of goal-directed behaviors will provide insight into the etiology of such disorders
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