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

Abstract

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 modelling to show that these dynamics reflect the speeded decision-making mechanisms used by humans and non-human 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.

Pathways to the persistence of drug use despite its adverse consequences

“…Field et al [ 80 ] have shown that these process models provide coherent explanations of drug choices as well as their remediation across recovery (see also [ 81 ]). This aligns with demonstrations that deliberative choice, including when evaluating the risk versus benefits of seeking rewards under punishment, is linked to medial prefrontal cortex [ 155 , 163 , 164 ] and its projections to thalamus [ 155 , 165 ]. These findings are relevant to evidence that training deliberative choice of non-alcohol rewards over alcohol reduces rates of relapse to alcohol drinking in the high-risk period following inpatient discharge [ 166 ].…”

“…Process models such as sequential sampling models (e.g., drift-diffusion [149] and linear ballistic accumulator [150]) provide computationally tractable decomposition of choice into its latent cognitive processes [37,[151][152][153]. These models identify computational similarities [154] between human [151], non-human primate [151], and rodent [155] choice. They have parallels to circuit function [156][157][158][159][160], holding promise for achieving a formal understanding of how value is used when making drug choices [81,161], complementing reinforcement learning models for learning this value [149,162].…”

The mediodorsal thalamus supports adaptive responding based on stimulus-outcome associations

“…These functional considerations have possible relevance to further highlight the highly integrative role played by the OFC ( Banerjee et al, 2020 ; Groman et al, 2019 ; Wang and Kahnt, 2021 ). Gaining a more systematic understanding of returning corticothalamic projections may be key to further advance our understanding of the functional principles at play within the thalamocortical architecture ( Alcaraz et al, 2018 ; Choi et al, 2022 ; Harris et al, 2019 ).…”

The Switchmaze: an open-design device for measuring motivation and drive switching in mice

“…Behavioural flexibility is typically studied in mice using approach/avoid decisions 13,14 or simplified set-shifting tasks under water deprivation and after arduous training regimens 10,11 . However, the fragmented nature of mouse behaviour complicates translational use of cognitive flexibility tasks like set-shifting [10][11][12] .…”