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Coordinated activity of ventral tegmental neurons adapts to appetitive and aversive learning

Kim, Y and Wood, J and Moghaddam, B (2012) Coordinated activity of ventral tegmental neurons adapts to appetitive and aversive learning. PLoS ONE, 7 (1).

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Our understanding of how value-related information is encoded in the ventral tegmental area (VTA) is based mainly on the responses of individual putative dopamine neurons. In contrast to cortical areas, the nature of coordinated interactions between groups of VTA neurons during motivated behavior is largely unknown. These interactions can strongly affect information processing, highlighting the importance of investigating network level activity. We recorded the activity of multiple single units and local field potentials (LFP) in the VTA during a task in which rats learned to associate novel stimuli with different outcomes. We found that coordinated activity of VTA units with either putative dopamine or GABA waveforms was influenced differently by rewarding versus aversive outcomes. Specifically, after learning, stimuli paired with a rewarding outcome increased the correlation in activity levels between unit pairs whereas stimuli paired with an aversive outcome decreased the correlation. Paired single unit responses also became more redundant after learning. These response patterns flexibly tracked the reversal of contingencies, suggesting that learning is associated with changing correlations and enhanced functional connectivity between VTA neurons. Analysis of LFP recorded simultaneously with unit activity showed an increase in the power of theta oscillations when stimuli predicted reward but not an aversive outcome. With learning, a higher proportion of putative GABA units were phase locked to the theta oscillations than putative dopamine units. These patterns also adapted when task contingencies were changed. Taken together, these data demonstrate that VTA neurons organize flexibly as functional networks to support appetitive and aversive learning. © 2012 Kim et al.


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Item Type: Article
Status: Published
CreatorsEmailPitt UsernameORCID
Kim, Y
Wood, Jjtw22@pitt.eduJTW22
Moghaddam, Bbita@pitt.eduBITA
Date: 6 January 2012
Date Type: Publication
Journal or Publication Title: PLoS ONE
Volume: 7
Number: 1
DOI or Unique Handle: 10.1371/journal.pone.0029766
Schools and Programs: Dietrich School of Arts and Sciences > Neuroscience
Refereed: Yes
MeSH Headings: Adaptation, Biological--physiology; Animals; Appetite--physiology; Appetitive Behavior--physiology; Association Learning--physiology; Avoidance Learning--physiology; Behavior, Animal--physiology; Dopaminergic Neurons--physiology; Learning--physiology; Male; Models, Biological; Rats; Rats, Sprague-Dawley; Reward; Ventral Tegmental Area--cytology; Ventral Tegmental Area--physiology
Other ID: NLM PMC3253108
PubMed Central ID: PMC3253108
PubMed ID: 22238652
Date Deposited: 03 Aug 2012 15:48
Last Modified: 25 Jan 2019 21:55


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