Midbrain dopamine neurons compute inferred and cached value prediction errors in a common framework
- National Institutes of Health, United States
Abstract
Midbrain dopamine neurons have been proposed to signal reward prediction errors as defined in temporal difference (TD) learning algorithms. While these models have been extremely powerful in interpreting dopamine activity, they typically do not use value derived through inference in computing errors. This is important because much real world behavior - and thus many opportunities for error-driven learning - is based on such predictions. Here, we show that error-signaling rat dopamine neurons respond to the inferred, model-based value of cues that have not been paired with reward and do so in the same framework as they track the putative cached value of cues previously paired with reward. This suggests that dopamine neurons access a wider variety of information than contemplated by standard TD models and that, while their firing conforms to predictions of TD models in some cases, they may not be restricted to signaling errors from TD predictions.
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Ethics
Animal experimentation: Experiments were performed at the National Institute on Drug Abuse Intramural Research Program in accordance with NIH guidelines and an approved institutional animal care and use committee protocol (15-CNRB-108). The protocol was approved by the ACUC at NIDA-IRP (Assurance Number: A4149-01).
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This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
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Midbrain dopamine neurons compute inferred and cached value prediction errors in a common framework
eLife 5:e13665.
https://doi.org/10.7554/eLife.13665
Further reading
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- Neuroscience
Evidence increasingly suggests that dopaminergic neurons play a more sophisticated role in predicting rewards than previously thought.
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Neurons generate and propagate electrical pulses called action potentials which annihilate on arrival at the axon terminal. We measure the extracellular electric field generated by propagating and annihilating action potentials and find that on annihilation, action potentials expel a local discharge. The discharge at the axon terminal generates an inhomogeneous electric field that immediately influences target neurons and thus provokes ephaptic coupling. Our measurements are quantitatively verified by a powerful analytical model which reveals excitation and inhibition in target neurons, depending on position and morphology of the source-target arrangement. Our model is in full agreement with experimental findings on ephaptic coupling at the well-studied Basket cell-Purkinje cell synapse. It is able to predict ephaptic coupling for any other synaptic geometry as illustrated by a few examples.
