Hypothalamic Interactions with Large-Scale Neural Circuits Underlying Reinforcement Learning and Motivated Behavior

Biological agents adapt behavior to support the survival needs of the individual and the species. In this review we outline the anatomical, physiological, and computational processes that support reinforcement learning (RL). We describe two circuits in the primate brain that are linked to specific aspects of learning and goal-directed behavior. The ventral circuit, that includes the amygdala, ventral medial prefrontal cortex, and ventral striatum, has substantial connectivity with the hypothalamus. The dorsal circuit, that includes inferior parietal cortex, dorsal lateral prefrontal cortex, and the dorsal striatum, has minimal connectivity with the hypothalamus. The hypothalamic connectivity suggests distinct roles for these circuits. We propose that the ventral circuit defines behavioral goals, and the dorsal circuit orchestrates behavior to achieve those goals. We propose that the neural circuitry that underlies goal-directed behavior in primates is organized into two large-scale, cortical/subcortical neural systems, which we refer to as the dorsal and ventral circuits.The ventral circuit, owing to substantial visual input from the medial temporal cortex and connectivity with the hypothalamus, learns about and identifies need-specific goal objects in the environment.The dorsal circuit, owing to substantial parietal cortex input, represents spatial metrics relevant to actions. The dorsal circuit uses these representations to generate actions on the fly (i.e., in the moment) to obtain goal objects.RL provides a framework for modeling these separate functions of the dorsal and ventral circuits. The ventral circuit represents states (internal and external) and state values, whereas the dorsal circuit computes actions on the fly to obtain goal states, which have been identified by the ventral circuit.