Triple Dissociation of Information Processing in Dorsal Striatum, Ventral Striatum, and Hippocampus on a Learned Spatial Decision Task

Abstract

Summary Decision-making studies across different domains suggest that decisions can arise from multiple, parallel systems in the brain: a flexible system utilizing action-outcome expectancies, and a more rigid system based on situation-action associations. The hippocampus, ventral striatum and dorsal striatum make unique contributions to each system, but how information processing in each of these structures supports these systems is unknown. Recent work has shown covert representations of future paths in hippocampus, and of future rewards in ventral striatum. We developed new analyses in order to use a comparative methodology and apply the same analyses to all three structures. Covert representations of future paths and reward were both absent from the dorsal striatum. In contrast, dorsal striatum slowly developed situation representations that selectively represented action-rich parts of the task. This triple dissociation suggests that the different roles these structures play are due to differences in information processing mechanisms.

Striatum processes reward differently in adolescents versus adults

“…Both groups had units that became activated at the beginning of trials, briefly inhibited at the instrumental response, and then activated again. Among these, consistent with other studies, adult units were reactivated earlier and returned to baseline before reward (24,25). The activation of their adolescent counterparts, in contrast, persisted all of the way to the time of reward retrieval.…”

“…Although others have previously observed prereward activity in the DS (24)(25)(26), the critical point here is that adolescents and adults have a different balance and time course in their patterns of such activity. The striatum is thought to play a direct role in situation-action associations (25) and may serve as the actor in an "actor-critic" model for biasing behavior toward more advantageous actions (27). The striatum receives dopamine Adults briefly ramped up their proportion of activated units at the instrumental poke and just before food trough entry, and these increases were not as strong in adolescents.…”

Conflict between place and response navigation strategies: Effects on vicarious trial and error (VTE) behaviors

“…There is the computationally slow, but flexible, deliberative system and the computationally fast, but inflexible, habit system (for review, see van der Meer et al 2012). In humans, deliberative decision-making encompasses several steps: exploring and recognizing the environment, imagining and predicting possible routes, evaluating their respective outcomes, and finally making the choice to take action.…”

“…Neurophysiological studies support the hypothesis that during VTE an animal is using its "cognitive map" by internally representing potential pathways (Johnson and Redish 2007) and evaluating future outcomes (van der Meer and Redish 2010). Various studies have shown that VTE is supported by the hippocampus (Hu and Amsel 1995;Voss et al 2011), occurs early in learning (Tolman 1939;van der Meer and Redish 2010), and increases with changes in task demands (Blumenthal et al 2011). However, to date, it has been difficult to determine the degree to which VTE behavior is linked to the different decisionmaking systems available.…”

Vision, Reanimated and Reimagined

“…The columnar cortical architecture seems to be wellsuited for unsupervised learning and for the distillation of its results into a long-term memory representation of the statistics of the world, as envisioned by Marr (1970). At the same time, reinforcement learning relies on the distinct architecture of the hippocampal formation, which appears to help the rest of the brain address the structural credit assignment problem, and of the cortico-striatal loops, which are involved in temporal credit assignment and action selection (e.g., Atallah, Frank, and O'Reilly, 2004;van der Meer, Johnson, Schmitzer Torbert, and Redish, 2010). The interactions among all these cognitive processes, all of which are active in an awake brain at all times, must be understood before a complete picture of what it means to see can emerge.…”