Over the river, through the woods: cognitive maps in the hippocampus and orbitofrontal cortex

Abstract

The hippocampus and the orbitofrontal cortex (OFC) both have important roles in cognitive processes such as learning, memory and decision making. Nevertheless, research on the OFC and hippocampus has proceeded largely independently, and little consideration has been given to the importance of interactions between these structures. Here, evidence is reviewed that the hippocampus and OFC encode parallel, but interactive, cognitive 'maps' that capture complex relationships between cues, actions, outcomes and other features of the environment. A better understanding of the interactions between the OFC and hippocampus is important for understanding the neural bases of flexible, goal-directed decision making.

Figure 1. Hippocampal and orbitofrontal cognitive mapping

a | In spatial tasks, many hippocampal neurons exhibit spatially specific firing. The firing fields (place fields, represented in the image by coloured ellipsoids) of these ‘place cells’ tile the environment. At an ensemble level, the firing of place cells encodes the animal’s position in the environment. b | In a reinforcement-learning framework, the ensemble firing of spatially tuned place cells could be thought of as encoding an environmental state space: that is, it would represent both individual states (the circumscribed portions of the environment within which each individual place cell is most active) and how they connect to one another. States in this example environmental state space are coloured to correspond to the place fields shown in part a. c | As animals traverse the environment, the activity of hippocampel neurons could be thought of as representing trajectories through the environmental state space. The figure shows raster plots that illustrate the firing of seven individual hippocampal cells representing two different state space trajectories (coloured to match parts a. and b.). The trajectories overlap as the animal travels along the central arm of a T-maze but diverge for left and right turns. Different sets of place cells represent positions to the left and right of the choice point. In a similar manner, the activity of non-spatially tuned hippocampal neurons could represent position in a more abstract, non-spatial state space. d | Similarly, as animals are engaged in decision- making tasks, orbitofrontal cortex (OFC) neurons that are active during the performance of actions or other task events (such as the presentation of cues and outcomes) could encode the current task state. e In contrast to the example state space shown in part b, which was defined entirely by position in the environment, the state space for an operant decision- making task might be structured around important task events, include ing actions (such as making an initial nose poke in an odour sample port). cues (such as the presentation of an odour) and outcomes (such as the delivery of a liquid reward). In these examples, the states represented might be the ‘odour-sampling state’ or the ‘reward-delivery state’. f | Because different OFC neurons are activated by specific actions and events (for example, they fire in response to particular odour cues rather than to general odour presentation), the trajectories through state space encoded by OFC ensembles vary depending on the animal’s actions (in this case, a left or right response) and on the information received from the environment.

Figure 2. Cognitive maps in action

a | In the T-maze decision-making task, animals learn by trial and error that a particular pattern of choices (for example, always turn left at the choice point) will be rewarded. b | When animals deliberate over their options at the choice point, hippocampal ensembles simulate spatial trajectories towards potential reward sites. At the same time, reward-sensitive neurons in the orbitofrontal cortex (OFC) become active. It has been proposed that these neurons are engaged in outcome simulation, potentially providing a substrate for the evaluation of action plans represented by hippocampal ensembles. c | In the sensory-preconditioning task (as depicted on the top row), animals learn a predictive relationship between two neutral stimuli, such as tones, during the preconditioning phase. During the conditioning phase of this task, one of these stimuli is paired with reward. In test sessions, animals responded to the preconditioned cue that, although never directly paired with reward, predicts the occurrence of the conditioned cue. This behaviour has been likened to inference, as animals seem to correctly derive the implicit causal structure of the task (that is, tone A is followed by tone B, which is followed by a reward) despite never having directly experienced this arrangement. Lesion and inactivation data suggest a potential neural model of this task (as depicted on the bottom row) in which hippocampal ensembles encode the relationships between elemental stimuli during the preconditioning and conditioning phases of the task, and this information is accessed by the OFC to support responding during the test session.