Neuron-type specific signals for reward and punishment in the ventral tegmental area

By Jeremiah Y. Cohen, Sebastian Haesler, Linh Vong, Bradford B. Lowell, Naoshige Uchida. 2012

584 citations recorded by the source corpus.

Dopamine has a central role in motivation and reward. Dopaminergic neurons in the ventral tegmental area (VTA) signal the discrepancy between expected and actual rewards (that is, reward prediction error), but how they compute such signals is unknown. We recorded the activity of VTA neurons while mice associated different odour cues with appetitive and aversive outcomes. We found three types of neuron based on responses to odours and outcomes: approximately half of the neurons (type I, 52%) showed phasic excitation after reward-predicting odours and rewards in a manner consistent with reward prediction error coding; the other half of neurons showed persistent activity during the delay between odour and outcome that was modulated positively (type II, 31%) or negatively (type III, 18%) by the value of outcomes. Whereas the activity of type I neurons was sensitive to actual outcomes (that is, when the reward was delivered as expected compared to when it was unexpectedly omitted), the activity of type II and type III neurons was determined predominantly by reward-predicting odours. We ‘tagged’ dopaminergic and GABAergic neurons with the light-sensitive protein channelrhodopsin-2 and identified them based on their responses to optical stimulation while recording. All identified dopaminergic neurons were of type I and all GABAergic neurons were of type II. These results show that VTA GABAergic neurons signal expected reward, a key variable for dopaminergic neurons to calculate reward prediction error.

Subfields: Cellular and Molecular Neuroscience, Molecular Biology, Sensory Systems

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Citations in the corpus

Coordinated and Compartmentalized Neuromodulation Shapes Sensory Processing in Drosophila (2015, positive): “Intriguingly, midbrain dopaminergic neurons responsive to punishment and reward also project to distinct targets in the mammalian brain and display a similar functional opponency as a consequence of reciprocal network interactions (Cohen et al., 2012; Lammel et al., 2012, 2014; Lerner et al., 2015).”
Dopamine neurons encoding long-term memory of object value for habitual behavior (2015, unknown): “Update-type neurons apparently correspond to the RPE-sensitive DA neurons that have been investigated repeatedly in various animal species including humans (Cohen et al., 2012; D'Ardenne et al., 2008; Schultz, 1998).”
Reward signal in a recurrent circuit drives appetitive long-term memory formation (2015, unknown): “In both vertebrates and invertebrates, the activity of reinforcement neurons is modified upon associative learning (Hammer, 1993; Mirenowicz and Schultz, 1994; Riemensperger et al., 2005; Cohen et al., 2012; Schultz, 2013).”
Neurophysiology of performance monitoring and adaptive behavior. (2014, background): “Recent evidence suggesting that GABAergic VTA neurons projecting to the prefrontal cortex (75) and ventral striatum may play a role in coding RPE and aversive outcomes (95, 548) may hint to an PERFORMANCE MONITORING AND ADAPTIVE BEHAVIOR”
How Prediction Errors Shape Perception, Attention, and Motivation (2012, background): “Such punishment PEs are also observed in the VTA, possibly resulting from projections from the lateral habenula to VTA GABAergic neurons (Cohen et al., 2012).”
Input-specific control of reward and aversion in the ventral tegmental area (2012, unknown): “Although VTA DA neurons play a role in reward-dependent behaviors 1-3, 7, 10, 12, 14, 31, 32 and inhibition of VTA DA neurons by GABAergic neurons contributes to reward prediction error calculations and promotes behaviors associated with aversion 10, 12, 13, 15 , the detailed circuits within the…”
A computational and neural model of momentary subjective well-being (2014, background): “Our key finding is that happiness is related to quantities associated with temporal difference errors that phasic dopamine release is thought to represent, errors that signal changes in long-term expected reward (17 – 19 , 39 – 41).”
Reward and aversion in a heterogeneous midbrain dopamine system (2013, unknown): “Indeed, it is wellestablished that aversive, stressful and salient events can excite midbrain DA neurons and cause DA release in target structures (Abercrombie et al., 1989; Anstrom and Woodward, 2005; Bassareo et al., 2002; Brischoux et al., 2009; Bromberg-Martin et al., 2010; Cohen et al., 2012; G”
Whole-brain mapping of direct inputs to midbrain dopamine neurons. (2012, unknown): “Dopamine neurons in the ventral tegmental area (VTA) and substantia nigra pars compacta (SNc) play pivotal roles in various brain functions including motivation, reinforcement learning, and motor control (Cohen et al., 2012; Ikemoto, 2007; Redgrave and Gurney, 2006; Schultz, 2007; Wise, 2004).”
Dopamine and Cognitive Control in Prefrontal Cortex. (2019, background): “However, during the delay, for instance between a conditioned stimulus and reward delivery, dopamine neurons are not active [153,154].”