Signed and unsigned reward prediction errors dynamically enhance learning and memory.
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ABSTRACT:
SUBMITTER: Rouhani N
PROVIDER: S-EPMC8041467 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:We remember when things change. Particularly salient are experiences where there is a change in rewards, eliciting reward prediction errors (RPEs). How do RPEs influence our memory of those experiences? One idea is that this signal directly enhances the encoding of memory. Another, not mutually exclusive, idea is that the RPE signals a deeper change in the environment, leading to the mnemonic separation of subsequent experiences from what came before, thereby creating a new latent context and a more separate memory trace. We tested this in four experiments where participants learned to predict rewards associated with a series of trial-unique images. High-magnitude RPEs indicated a change in the underlying distribution of rewards. To test whether these large RPEs created a new latent context, we first assessed recognition priming for sequential pairs that included a high-RPE event or not (Exp. 1: n = 27 & Exp. 2: n = 83). We found evidence of recognition priming for the high-RPE event, indicating that the high-RPE event is bound to its predecessor in memory. Given that high-RPE events are themselves preferentially remembered (Rouhani, Norman, & Niv, 2018), we next tested whether there was an event boundary across a high-RPE event (i.e., excluding the high-RPE event itself; Exp. 3: n = 85). Here, sequential pairs across a high RPE no longer showed recognition priming whereas pairs within the same latent reward state did, providing initial evidence for an RPE-modulated event boundary. We then investigated whether RPE event boundaries disrupt temporal memory by asking participants to order and estimate the distance between two events that had either included a high-RPE event between them or not (Exp. 4). We found (n = 49) and replicated (n = 77) worse sequence memory for events across a high RPE. In line with our recognition priming results, we did not find sequence memory to be impaired between the high-RPE event and its predecessor, but instead found worse sequence memory for pairs across a high-RPE event. Moreover, greater distance between events at encoding led to better sequence memory for events across a low-RPE event, but not a high-RPE event, suggesting separate mechanisms for the temporal ordering of events within versus across a latent reward context. Altogether, these findings demonstrate that high-RPE events are both more strongly encoded, show intact links with their predecessor, and act as event boundaries that interrupt the sequential integration of events. We captured these effects in a variant of the Context Maintenance and Retrieval model (CMR; Polyn, Norman, & Kahana, 2009), modified to incorporate RPEs into the encoding process.
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Project description:Theories of instrumental learning are centred on understanding how success and failure are used to improve future decisions. These theories highlight a central role for reward prediction errors in updating the values associated with available actions. In animals, substantial evidence indicates that the neurotransmitter dopamine might have a key function in this type of learning, through its ability to modulate cortico-striatal synaptic efficacy. However, no direct evidence links dopamine, striatal activity and behavioural choice in humans. Here we show that, during instrumental learning, the magnitude of reward prediction error expressed in the striatum is modulated by the administration of drugs enhancing (3,4-dihydroxy-L-phenylalanine; L-DOPA) or reducing (haloperidol) dopaminergic function. Accordingly, subjects treated with L-DOPA have a greater propensity to choose the most rewarding action relative to subjects treated with haloperidol. Furthermore, incorporating the magnitude of the prediction errors into a standard action-value learning algorithm accurately reproduced subjects' behavioural choices under the different drug conditions. We conclude that dopamine-dependent modulation of striatal activity can account for how the human brain uses reward prediction errors to improve future decisions.
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