Thalamocortical and corticothalamic pathways differentially contribute to goal-directed behaviors in the rat

Abstract

Highly distributed neural circuits are thought to support adaptive decision-making in volatile and complex environments. Notably, the functional interactions between prefrontal and reciprocally connected thalamic nuclei areas may be important when choices are guided by current goal value or action-outcome contingency. We examined the functional involvement of selected thalamocortical and corticothalamic pathways connecting the dorsomedial prefrontal cortex (dmPFC) and the mediodorsal thalamus (MD) in the behaving rat. Using a chemogenetic approach to inhibit projection-defined dmPFC and MD neurons during an instrumental learning task, we show that thalamocortical and corticothalamic pathways differentially support goal attributes. Both pathways participate in adaptation to the current goal value, but only thalamocortical neurons are required to integrate current causal relationships. These data indicate that antiparallel flow of information within thalamocortical circuits may convey qualitatively distinct aspects of adaptive decision-making and highlight the importance of the direction of information flow within neural circuits.

eLife digest

Planning and decision-making rely upon a region of the brain called the prefrontal cortex. But the prefrontal cortex does not act in isolation. Instead, it works together with a number of other brain regions. These include the thalamus, an area long thought to pass information on to the cortex for further processing. But signals also travel in the opposite direction, from the cortex back to the thalamus. Does the cortex-to-thalamus pathway carry the same information as the thalamus-to-cortex pathway?

To find out, Alcaraz et al. blocked each pathway in rats performing a decision-making task. The rats had learned that pressing a lever led to one type of reward, whereas moving a rod led to another. Alcaraz et al. reduced the desirability of one of the rewards by giving the rats free access to it for an hour. Afterwards, the rats opted mainly for the action associated with the reward that had remained desirable. However, blocking either the thalamus-to-cortex or cortex-to-thalamus pathway prevented this preference from emerging. This suggests that an information flow in both directions is necessary to update knowledge about the value of a reward.

In a second experiment, Alcaraz et al. removed the link between one of the actions and its reward. The reward instead appeared at random, irrespective of the rat’s own behavior. Control rats responded by focusing their efforts on the action that still delivered a reliable reward, and by performing the other action less often. Blocking the thalamus-to-cortex pathway prevented this response, but blocking the cortex-to-thalamus pathway did not. This suggests that only the former pathway is necessary to re-evaluate the relationship between an action and an outcome.

Two key aspects of goal-directed behavior – recognizing the value of a reward and the link between an action and an outcome – thus depend differently on the thalamus-to-cortex and cortex-to-thalamus pathways. This same principle may also be at work in other neural circuits with bidirectional connections. Understanding such principles may lead to better strategies for treating disorders of brain connectivity, such as schizophrenia.