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Research Articles, Behavioral/Cognitive

Corticolimbic Mechanisms of Behavioral Inhibition under Threat of Punishment

Jeroen P.H. Verharen, Mauri W. van den Heuvel, Mieneke Luijendijk, Louk J.M.J. Vanderschuren and Roger A.H. Adan
Journal of Neuroscience 29 May 2019, 39 (22) 4353-4364; DOI: https://doi.org/10.1523/JNEUROSCI.2814-18.2019
Jeroen P.H. Verharen
1Brain Center Rudolf Magnus, Department of Translational Neuroscience, University Medical Center Utrecht, 3584CG Utrecht, The Netherlands,
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, 3584 CM, Utrecht, The Netherlands, and
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Mauri W. van den Heuvel
1Brain Center Rudolf Magnus, Department of Translational Neuroscience, University Medical Center Utrecht, 3584CG Utrecht, The Netherlands,
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Mieneke Luijendijk
1Brain Center Rudolf Magnus, Department of Translational Neuroscience, University Medical Center Utrecht, 3584CG Utrecht, The Netherlands,
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Louk J.M.J. Vanderschuren
2Department of Animals in Science and Society, Division of Behavioural Neuroscience, Faculty of Veterinary Medicine, Utrecht University, 3584 CM, Utrecht, The Netherlands, and
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Roger A.H. Adan
1Brain Center Rudolf Magnus, Department of Translational Neuroscience, University Medical Center Utrecht, 3584CG Utrecht, The Netherlands,
3Institute of Physiology and Neuroscience, Sahlgrenska Academy at the University of Gothenburg, 413-90, Gothenburg, Sweden
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Abstract

Being able to limit the pursuit of reward to prevent negative consequences is an important expression of behavioral inhibition. Everyday examples of an inability to exert such control over behavior are the overconsumption of food and drugs of abuse, which are important factors in the development of obesity and addiction, respectively. Here, we use a behavioral task that assesses the ability of male rats to exert behavioral restraint at the mere sight of palatable food during the presentation of an audiovisual threat cue to investigate the corticolimbic underpinnings of behavioral inhibition. We demonstrate a prominent role for the medial prefrontal cortex in the exertion of control over behavior under threat of punishment. Moreover, task engagement relies on function of the ventral striatum, whereas the basolateral amygdala mediates processing of the threat cue. Together, these data show that inhibition of reward pursuit requires the coordinated action of a network of corticolimbic structures.

SIGNIFICANCE STATEMENT There is a need for translational models that allow to dissect mechanisms underlying the processes involved in controlling behavior. In this study, we present a novel behavioral task that assesses the ability of rats to exert behavioral restraint over the consumption of a visually present sucrose pellet during the presentation of an audiovisual threat cue. This task requires relatively little behavioral training and it discerns distinct behavioral impairments, including a failure to retrieve stimulus value, a reduced task engagement, and compromised inhibition of behavior. Using pharmacological inactivations of different regions of the corticolimbic system of the rat, we demonstrate dissociable roles for the prefrontal cortex, amygdala, and striatum in inhibition of reward pursuit under threat of punishment.

  • corticolimbic
  • inhibition
  • punishment
  • reward
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The Journal of Neuroscience: 39 (22)
Journal of Neuroscience
Vol. 39, Issue 22
29 May 2019
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Corticolimbic Mechanisms of Behavioral Inhibition under Threat of Punishment
Jeroen P.H. Verharen, Mauri W. van den Heuvel, Mieneke Luijendijk, Louk J.M.J. Vanderschuren, Roger A.H. Adan
Journal of Neuroscience 29 May 2019, 39 (22) 4353-4364; DOI: 10.1523/JNEUROSCI.2814-18.2019

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Corticolimbic Mechanisms of Behavioral Inhibition under Threat of Punishment
Jeroen P.H. Verharen, Mauri W. van den Heuvel, Mieneke Luijendijk, Louk J.M.J. Vanderschuren, Roger A.H. Adan
Journal of Neuroscience 29 May 2019, 39 (22) 4353-4364; DOI: 10.1523/JNEUROSCI.2814-18.2019
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Keywords

  • corticolimbic
  • inhibition
  • punishment
  • reward

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