A Corticothalamic Circuit Trades off Speed for Safety during Decision-Making under Motivational Conflict

• Published in: The Journal of neuroscience 2022-04, Vol.42 (16), p.3473-3483
• Main Authors: Choi, Eun A, Husić, Medina, Millan, E Zayra, Gilchrist, Sophia, Power, John M, Jean-Richard Dit Bressel, Philip, McNally, Gavan P
• Format: Article
• Language: English
• Subjects: Animals; Calcium imaging; Cognitive ability; Decision analysis; Decision making; Decision Making - physiology; Health risks; Impulsive Behavior; Male; Mice; Motivation; Neuroimaging; Prefrontal Cortex; Reward; Safety; Thalamus
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/JNEUROSCI.0088-22.2022

Decisions to act while pursuing goals in the presence of danger must be made quickly but safely. Premature decisions risk injury or death, whereas postponing decisions risk goal loss. Here we show how mice resolve these competing demands. Using microstructural behavioral analyses, we identified the spatiotemporal dynamics of approach-avoidance decisions under motivational conflict in male mice. Then we used cognitive modeling to show that these dynamics reflect the speeded decision-making mechanisms used by humans and nonhuman primates, with mice trading off decision speed for safety of choice when danger loomed. Using calcium imaging in paraventricular thalamus and optogenetic inhibition of the prelimbic cortex to paraventricular thalamus pathway, we show that this speed-safety trade off occurs because increases in paraventricular thalamus activity increase decision caution, thereby increasing approach-avoid decision times in the presence of danger. Our findings demonstrate that a discrete brain circuit involving the paraventricular thalamus and its prefrontal input adjusts decision caution during motivational conflict, trading off decision speed for decision safety when danger is close. We identify the corticothalamic pathway as central to cognitive control during decision-making under conflict. Foraging animals balance the need to seek food and energy against the conflicting needs to avoid injury and predation. This competition is fundamental to survival but rarely has a stable, correct solution. Here we show that approach-avoid decisions under motivational conflict involve strategic adjustments in decision caution controlled via a top-down corticothalamic pathway from the prelimbic cortex to the paraventricular thalamus. We identify a novel corticothalamic mechanism for cognitive control that is applicable across a range of motivated behaviors and mark paraventricular thalamus and its prefrontal cortical input as targets to remediate the deficits in decision caution characteristic of unsafe and impulsive choices.