Learning, memory and consolidation mechanisms for behavioral control in hierarchically organized cortico-basal ganglia systems

This article aims to provide a synthesis on the question how brain structures cooperate to accomplish hierarchically organized behaviors, characterized by low-level, habitual routines nested in larger sequences of planned, goal-directed behavior. The functioning of a connected set of brain structures-prefrontal cortex, hippocampus, striatum, and dopaminergic mesencephalon-is reviewed in relation to two important distinctions: (a) goal-directed as opposed to habitual behavior and (b) model-based and model-free learning. Recent evidence indicates that the orbitomedial prefrontal cortices not only subserve goal-directed behavior and model-based learning, but also code the landscape (task space) of behaviorally relevant variables. While the hippocampus stands out for its role in coding and memorizing world state representations, it is argued to function in model-based learning but is not required for coding of action-outcome contingencies, illustrating that goal-directed behavior is not congruent with model-based learning. While the dorsolateral and dorsomedial striatum largely conform to the dichotomy between habitual versus goal-directed behavior, ventral striatal functions go beyond this distinction. Next, we contextualize findings on coding of reward-prediction errors by ventral tegmental dopamine neurons to suggest a broader role of mesencephalic dopamine cells, viz. in behavioral reactivity and signaling unexpected sensory changes. We hypothesize that goal-directed behavior is hierarchically organized in interconnected cortico-basal ganglia loops, where a limbic-affective prefrontal-ventral striatal loop controls action selection in a dorsomedial prefrontal-striatal loop, which in turn regulates activity in sensorimotor-dorsolateral striatal circuits. This structure for behavioral organization requires alignment with mechanisms for memory formation and consolidation. We propose that frontal corticothalamic circuits form a high-level loop for memory processing that initiates and temporally organizes nested activities in lower-level loops, including the hippocampus and the ripple-associated replay it generates. The evidence on hierarchically organized behavior converges with that on consolidation mechanisms in suggesting a frontal-to-caudal directionality in processing control.