A Causal Link Between Prediction Errors, Dopamine Neurons and Learning

By Elizabeth E Steinberg, R. Keiflin, Josiah R. Boivin, Ilana B. Witten, Karl Deisseroth, P. Janak. Nature Neuroscience, 2013

874 citations recorded by the source corpus.

Situations in which rewards are unexpectedly obtained or withheld represent opportunities for new learning. Often, this learning includes identifying cues that predict reward availability. Unexpected rewards strongly activate midbrain dopamine neurons. This phasic signal is proposed to support learning about antecedent cues by signaling discrepancies between actual and expected outcomes, termed a reward prediction error. However, it is unknown whether dopamine neuron prediction error signaling and cue-reward learning are causally linked. To test this hypothesis, we manipulated dopamine neuron activity in rats in two behavioral procedures, associative blocking and extinction, that illustrate the essential function of prediction errors in learning. We observed that optogenetic activation of dopamine neurons concurrent with reward delivery, mimicking a prediction error, was sufficient to cause long-lasting increases in cue-elicited reward-seeking behavior. Our findings establish a causal role for temporally precise dopamine neuron signaling in cue-reward learning, bridging a critical gap between experimental evidence and influential theoretical frameworks.

Subfields: Cellular and Molecular Neuroscience, Cognitive Neuroscience, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/dbea8d412f5b68ef2abe19af5ae2b62246bcd47f

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Citations in the corpus

Three Ways That Non-associative Knowledge May Affect Associative Learning Processes (2016, background): “The concept of prediction error as a determinant of learning is thus closely linked to the blocking effect and furthermore, prediction error has been shown to be important if not indeed causal for blocking (Steinberg et al., 2013).”
Mesolimbic Dopamine Signals the Value of Work (2015, positive): “Further support for a link between phasic dopamine and RPE comes from measurements of dopamine release using fast-scan cyclic voltammetry (FSCV) 3,4 and optogenetic manipulations 5,6 .”
Neuronal Reward and Decision Signals: From Theories to Data. (2015, background): “Optogenetically induced nose poke learning occurs also with activation of dopamine axons in rat nucleus accumbens and is attenuated by intraaccumbens infusion of dopamine D1 and D2 receptor antagonists, suggesting involvement of dopamine projections to nucleus accumbens (562).”
Intact-Brain Analyses Reveal Distinct Information Carried by SNc Dopamine Subcircuits (2015, background): “…neurons suggested that a key function of DA is to transmit reward prediction error signals (Mirenowicz and Schultz, 1996; Schultz et al., 1997; Waelti et al., 2001), a hypothesis concordant with temporal difference learning models (Montague et al., 1996, 2004; Steinberg et al., 2013; Sutton, 1988).”
Synaptic Plasticity Forms and Functions. (2020, background): “The dependence of reward-motivated behavior on dopamine (DA) neuron activity and DA receptor activation is a well-documented example (Schultz 2007, Steinberg et al. 2013, Pignatelli & Bonci 2015, Berke 2018).”
Neural interactions in the human frontal cortex dissociate reward and punishment learning (2024, background): “…error (RPE) signals have been observed in the midbrain, ventral striatum and ventromedial prefrontal cortex (vmPFC) (Schultz et al., 1997; O’Doherty et al., 2001, 2004; Pessiglione et al., 2006; D’Ardenne et al., 2008; Steinberg et al., 2013; Palminteri et al., 2015; Gueguen et al., 2021).”