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Navigating for reward

A Publisher Correction to this article was published on 23 July 2021

This article has been updated

Abstract

An organism’s survival can depend on its ability to recall and navigate to spatial locations associated with rewards, such as food or a home. Accumulating research has revealed that computations of reward and its prediction occur on multiple levels across a complex set of interacting brain regions, including those that support memory and navigation. However, how the brain coordinates the encoding, recall and use of reward information to guide navigation remains incompletely understood. In this Review, we propose that the brain’s classical navigation centres — the hippocampus and the entorhinal cortex — are ideally suited to coordinate this larger network by representing both physical and mental space as a series of states. These states may be linked to reward via neuromodulatory inputs to the hippocampus–entorhinal cortex system. Hippocampal outputs can then broadcast sequences of states to the rest of the brain to store reward associations or to facilitate decision-making, potentially engaging additional value signals downstream. This proposal is supported by recent advances in both experimental and theoretical neuroscience. By discussing the neural systems traditionally tied to navigation and reward at their intersection, we aim to offer an integrated framework for understanding navigation to reward as a fundamental feature of many cognitive processes.

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Fig. 1: Modulations of hippocampal–entorhinal activity at reward-related behavioural timepoints.
Fig. 2: Dopaminergic signalling and innervation of the hippocampus.
Fig. 3: Hippocampal theta sequences and replay.
Fig. 4: Hypothesized interactions between brain systems in navigating to reward.

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Acknowledgements

The authors thank A. Mohebi for feedback on the manuscript, M.H. Plitt and T.G. Fisher for insightful discussions and E. Duvelle for helpful correspondence. This work was supported by the US Office of Naval Research (N00141812690), NIDA (DA042012), the Simons Foundation (542987SPI), the Vallee Foundation, the James S. McDonnell Foundation (L.M.G.) and the Helen Hay Whitney Foundation (M.S.).

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Correspondence to Marielena Sosa or Lisa M. Giocomo.

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Glossary

Grid cells

Entorhinal cortex cells that fire in triangularly spaced fields that tile the whole environment.

Place cells

Hippocampal cells that fire maximally in one or a few discrete regions of space (each cell’s ‘place field’).

Theta sequences

Sequential spikes of multiple place cells that together encode a trajectory through space, ordered by the theta phase of each spike. Theta sequences occur during times of high theta power, typically during movement.

Sharp-wave ripples

(SWRs). High-frequency oscillations (about 150–250 Hz) coincident with a sharp, low-frequency deflection in the local field potential. These events reflect the coincident activation of many hippocampal cells in a short period (about 50–200 ms) and typically occur during immobility.

Replay events

Sequential spikes of multiple place cells that typically occur locked to sharp-wave ripples during immobility and that together encode a trajectory through space. In high-fidelity replay events, place cells in the sequence are reactivated according to the order in which they fired during a previous run.

States

Snapshots of a situation discretizing a longer continuous process that comprises an experience. As an analogy, if this snapshot were taken by a camera, the duration of the state would be the exposure time and would vary depending on the situation (for example, how dark it is outside).

Value

How much an outcome, or state that predicts an outcome, is ‘worth’. This worth includes the amount and likelihood of the reward predicted.

Probabilistic value

The probability that a reward will be delivered given a certain choice. Even if a choice is correct according to the task, changing the probability of reward delivery can modulate the value of preceding states.

Cheeseboard maze

A spatial task in which rewards are hidden in a subset of holes or wells in the floor of an open arena. This task is used as a spatial memory paradigm because the animal has to remember which wells are rewarded on the basis of their position in the environment, and the reward locations can change across sessions or days.

Reward prediction error

(RPE). The difference between the reward received and the reward expected. Positive RPEs indicate larger rewards than expected (including a reward when none was expected), whereas negative RPEs indicate smaller rewards than expected (including the absence of a reward when it was expected).

Reinforcement learning

A set of computational theories often used for machine learning to describe how states and actions are assigned values that inform how an agent can receive the maximal reward.

Temporal difference reinforcement learning

(TD-RL). A type of reinforcement learning in which values are updated by a reward prediction error between temporally adjacent states, such that states preceding the reward receive a ‘cached’ value prediction.

Motivation

The impetus an agent feels to perform reward-seeking actions. Value is used to inform motivation and invigorate reward-seeking actions (make them faster and more efficient).

Value function

A function of adjacent states, or states paired with actions, that computes the expected future reward in each state.

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Sosa, M., Giocomo, L.M. Navigating for reward. Nat Rev Neurosci 22, 472–487 (2021). https://doi.org/10.1038/s41583-021-00479-z

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