Review
Dopamine and adaptive memory

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Memory is essential to adaptive behavior because it allows past experience to guide choices. Emerging findings indicate that the neurotransmitter dopamine, which signals motivationally important events, also modulates the hippocampus, a crucial brain system for long-term memory. Here we review recent evidence that highlights multiple mechanisms whereby dopamine biases memory towards events that are of motivational significance. These effects take place over a variety of timescales, permitting both expectations and outcomes to influence memory. Thus, dopamine ensures that memories are relevant and accessible for future adaptive behavior, a concept we refer to as ‘adaptive memory’. Understanding adaptive memory at biological and psychological levels helps to resolve a fundamental challenge in memory research: explaining what is remembered, and why.

Introduction

Memory is essential to behavior, enabling organisms to draw on past experience to improve choices and actions. Much research has focused on how the hippocampus builds accurate memory for past events. Emerging findings indicate that the neurotransmitter dopamine, known to play a key role in motivated behavior, has a direct impact on memory formation in the hippocampus. Here, we review this emerging literature that demonstrates that interactions between midbrain dopamine regions and the hippocampus promote memory for episodes that are rewarding and novel and build memory representations well-suited to guide later choices. By integrating findings from both human and animal research, we argue for a framework in which dopamine helps create enriched mnemonic representations of the environment to support adaptive behavior.

Section snippets

The hippocampus: Creating building blocks for memory-guided behavior

After decades of research, our understanding of the brain mechanisms that contribute to long-term memory for events or episodes – often referred to as episodic memory – has evolved significantly. Episodic memories are formed rapidly (after even a single experience) and are rich in contextual details. Episodic memories are also thought to be relational: they encode relationships between multiple elements of an event 1, 2. Extensive converging evidence indicates that episodic memory depends

Brain systems for learning and motivation

Converging evidence indicates that the release of dopamine signals motivationally important events and behaviors. Key findings come from a series of seminal neurophysiology studies of dopamine-containing midbrain neurons in primates receiving reward (for a review see [13]). In these studies, a monkey receives a reward (e.g. juice), which is predicted by a cue (e.g. a tone). Dopamine neurons respond with a burst of activity – often referred to as a phasic response – when the monkey unexpectedly

Dopamine modulates hippocampal memories

Much of the evidence for the role of dopamine in modulating hippocampal function comes from anatomical and electrophysiological studies in animals. Midbrain dopamine neurons project directly to the hippocampus and to the surrounding MTL cortices 24, 25 (Figure 2; see Table I in Box 2). Indeed, in animals, dopamine seems to be essential for hippocampal long-term memory. Studies in animals indicate that dopamine acting at hippocampal synapses is a necessary precursor not only for long-term

Dopamine modulates hippocampal memories over a range of timescales

Interestingly, the role of dopamine in supporting the formation of memories extends over a range of timescales: before, during, and after an event. As discussed in the next section, this broad range of timescales implies a similarly broad range of neurobiological mechanisms by which midbrain dopamine neurons can exert an effect on memory formation in the hippocampus.

Initial evidence highlighted the time period before an event as a window during which the presence of dopamine is crucial.

Putative neurobiological mechanisms: Tonic vs. phasic dopamine

The precise mechanisms whereby dopamine modulates memory formation in the hippocampus are not yet known. Nevertheless, existing findings point to a potentially important role for tonic responses in dopamine neurons. In particular, animal research indicates that hippocampal activity originating in the subiculum disinhibits midbrain dopamine neurons, thus increasing the number of tonically active cells, but does not produce phasic responses in individual neurons [63]. As detailed below, this key

Concluding remarks

To summarize, extensive evidence indicates that dopamine release before, during, and after an event supports hippocampal plasticity and episodic memory formation. Dopamine thus seems to influence which episodic memories are formed and how they are represented, enabling memory for past experience to support future adaptive behavior. We use the term ‘adaptive memory’ as a construct for this process to highlight the selectivity of memory and to consider whether this selectivity, which can seem

Acknowledgements

The authors are grateful to Lauren Atlas, Nathan Clement, Lila Davachi, Juliet Davidow, Karin Foerde, Elizabeth Johnson, Jeff Macinnes, Vishnu Murty, and G. Elliott Wimmer for insightful comments on an earlier draft.

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