Dopamine in motivational control: rewarding, aversive, and alerting

By Ethan S. Bromberg-Martin, Masayuki Matsumoto, Okihide Hikosaka. 2010

2,199 citations recorded by the source corpus.

SUMMARY Midbrain dopamine neurons are well known for their strong responses to rewards and their critical role in positive motivation. It has become increasingly clear, however, that dopamine neurons also transmit signals related to salient but non-rewarding experiences such as aversive and alerting events. Here we review recent advances in understanding the reward and non-reward functions of dopamine. Based on this data, we propose that dopamine neurons come in multiple types that are connected with distinct brain networks and have distinct roles in motivational control. Some dopamine neurons encode motivational value, supporting brain networks for seeking, evaluation, and value learning. Others encode motivational salience, supporting brain networks for orienting, cognition, and general motivation. Both types of dopamine neurons are augmented by an alerting signal involved in rapid detection of potentially important sensory cues. We hypothesize that these dopaminergic pathways for value, salience, and alerting cooperate to support adaptive behavior.

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

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Citations in the corpus

Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Dopaminergic pathways have been investigated extensively as part of a reinforcement system that motivates and modifies many facets of animal behavior (Beninger, 1983; Bromberg-Martin et al., 2010; Redgrave and Gurney, 2006; Schultz et al., 1997; Waddell, 2013; Wise, 2004).”
GABA Neurons of the VTA Drive Conditioned Place Aversion (2012, background): “Others encode motivational salience, supporting brain networks for orienting, cognition, and general motivation’’ (Bromberg-Martin et al., 2010a).”
Climbing fibers encode a temporal-difference prediction error during cerebellar learning in mice (2015, positive): “In theories of reinforcement learning based on the TD model, these dopamine responses are important for driving higher-order acquisition of approach behavior to potential reward 23,37,38,49,50 .”
The mysterious motivational functions of mesolimbic dopamine. (2012, positive): “For many years, it was thought that ventral tegmental DA neuron activity was not increased by aversive stimuli; however, recent studies have demonstrated that the electrophysiological activity of putative or identified DA neurons is increased by aversive or stressful conditions (Anstrom and Woodward”
Pain-relief learning in flies, rats, and man: basic research and applied perspectives (2014, methodology): “A similar picture may be emerging for mammals as well (Brischoux et al. 2009; Bromberg-Martin et al. 2010; Ilango et al. 2012; Lammel et al. 2012).”
Whole-brain mapping of direct inputs to midbrain dopamine neurons. (2012, neutral): “…the aforementioned findings indicate that dopamine neurons integrate diverse kinds of information, the mechanisms by which the firing of dopamine neurons is regulated in a behavioral context remain largely unknown (Bromberg-Martin et al., 2010; Lee and Tepper, 2009; Sesack and Grace, 2010).”
Competing dopamine neurons drive oviposition choice for ethanol in Drosophila (2013, background): “Interestingly, similar neural principles can be applied to motivational control of behavior in mammals, where dopamine neurons can also transmit signals related to rewarding and nonrewarding experiences (54).”
The Integration of Negative Affect, Pain, and Cognitive Control in the Cingulate Cortex (2011, background): “Interestingly, some neurons in the primate substantia nigra are activated by aversive stimuli and cues predicting their occurrenc”
Glutamate and dopamine in schizophrenia: an update for the 21st century (2015, background): “Animal studies provide support for dopamine’s role as a mediator in assigning motivational salience to internal or external stimuli, and thereby determining which stimuli grab attention and drive behaviour (Bromberg-Martin et al., 2010).”
Distinct dopamine receptor pathways underlie the temporal sensitivity of associative learning (2019, background): “Neural circuits involved in associative learning integrate sensory signals with rewarding or punishing reinforcement cues, frequently encoded by neuromodulatory dopaminergic neurons (DANs; Aso et al., 2014a; Bromberg-Martin et al., 2010; Lerner et al., 2015; Schultz et al., 1997; Waddell, 2016).”
Computational models of basal-ganglia pathway functions: focus on functional neuroanatomy (2013, background): “…that phasic dopamine signals in BG encode error signals of reward prediction (Hollerman and Schultz, 1998) and other salient unexpected events (e.g., Horvitz et al., 1997; Rebec, 1998), where value and salience of events might be signaled by distinct dopamine systems (Bromberg-Martin et al., 2010).”
Sweet Taste and Nutrient Value Subdivide Rewarding Dopaminergic Neurons in Drosophila (2015, background): “Dopaminergic neurons provide reward learning signals in mammals and insects [1–4].”