Integrating hippocampus and striatum in decision-making

Abstract

Learning and memory and navigation literatures emphasize interactions between multiple memory systems: a flexible, planning-based system and a rigid, cached-value system. This has profound implications for decision-making. Recent conceptualizations of flexible decision-making employ prospection and projection arising from a network involving the hippocampus. Recent recordings from rodent hippocampus in decision-making situations have found transient forward-shifted representations. Evaluation of that prediction and subsequent action-selection probably occurs downstream (e.g. in orbitofrontal cortex, in ventral and dorsomedial striatum). Classically, striatum has been identified as a crucial component of the less-flexible, incremental system. Current evidence, however, suggests that striatum is involved in both flexible and stimulus-response decision-making, with dorsolateral striatum involved in stimulus-response strategies and ventral and dorsomedial striatum involved in goal-directed strategies.

Fig 1. Decision-making under formulations of cache-based stimulus-action (A) and expectation-based planning (B) strategies

Both strategies require a situation-recognition component to produce a starting point S for predictions within the decision-making process. In cache-based models (A), decision-making entails selecting the action a with the maximum expected return E(V). This means that actions are judged only in terms of their cached expected return. In planning models (B), active memory processes allow exploration of potential future situations S₁, . . . , S₄. The outcome of each potential future E(S_i ) can then be compared to the animal’s current needs to determine the expected value E(V). Because planning systems include future situation predictions, it can remain flexible under conditions in which cache-systems remain rigid. However, because the planning system must serially search into possible futures, it will require processing time not required by the cache-system.

Fig 2. Vicarious trial and error

On the first example trial, the rat looks left and then goes right. On the second example trial, the rat looks right and then goes left. On the third example trial, the rat looks right, starts left, but then goes right. On the fourth example trial, the rat looks left before starting the journey down the central track and then does not pause at the actual choice point, suggesting the moment of decision may have been made before the journey down the central track in this last example. A video of a real rat running these four examples is shown in the supplemental movie.

Fig 3. Forward-shifted neural representations at the choice point

Spatial representations were decoded from the activity of simultaneously recorded neural ensembles within the CA3 region of the hippocampus. Each panel shows a sample of the decoded hippocampal spatial representation in a cued choice task [29]. Panels are arranged in 40msec intervals from left-to-right, then top-to-bottom. Representations are displayed as a probability distribution over space (red = high probability, blue = low probability) and the animal’s position is shown as a white ○. The representations closely tracked the rat’s position as the rat approached the choice point. As the rat paused at the choice point, hippocampal spatial representations moved forward of the animal into each arm (first to the left, then to the right). Forward-shifted neural representations provide a potential mechanism for consideration of future possibilities. Data is from another example from data set originally reported in [29].