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

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.SIGNIFICANCE STATEMENT 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.

Phasic inhibition of dopamine neurons is an instrumental punisher.

It is well established that the activity of VTA dopamine neurons is sufficient to serve as a Pavlovian reinforcer but whether this activity can also serve as instrumental reinforcer is less well understood. Here we studied the effects of optogenetic inhibition of VTA dopamine neurons in instrumental conditioning preparations. We show that optogenetic inhibition of VTA dopamine neurons causes a response-specific, contingency-sensitive suppression of instrumental responding. This suppression was due to instrumental response, not Pavlovian stimulus, learning and could not be attributed to deepened instrumental extinction learning. These effects of optogenetic inhibition of VTA dopamine neurons on instrumental responding are formally similar to the effects of aversive events in instrumental preparations and show that optogenetic inhibition of VTA dopamine neurons is sufficient to serve as an instrumental punisher. (PsycInfo Database Record (c) 2021 APA, all rights reserved).