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Featured ArticleArticles, Behavioral/Cognitive

Role of the Dorsal Medial Habenula in the Regulation of Voluntary Activity, Motor Function, Hedonic State, and Primary Reinforcement

Yun-Wei A. Hsu, Si D. Wang, Shirong Wang, Glenn Morton, Hatim A. Zariwala, Horacio O. de la Iglesia and Eric E. Turner
Journal of Neuroscience 20 August 2014, 34 (34) 11366-11384; DOI: https://doi.org/10.1523/JNEUROSCI.1861-14.2014
Yun-Wei A. Hsu
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
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Si D. Wang
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
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  • ORCID record for Si D. Wang
Shirong Wang
2Sanford-Burnham Medical Research Institute, La Jolla, California 92037,
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Glenn Morton
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
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Hatim A. Zariwala
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
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Horacio O. de la Iglesia
3Department of Biology, University of Washington, Seattle, Washington 98195-1800,
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Eric E. Turner
1Center for Integrative Brain Research, Seattle Children's Research Institute, Seattle, Washington 98101,
4Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, Washington 98195, and
5Center on Human Development and Disability, University of Washington, Seattle, Washington 98195
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Abstract

The habenular complex in the epithalamus consists of distinct regions with diverse neuronal populations. Past studies have suggested a role for the habenula in voluntary exercise motivation and reinforcement of intracranial self-stimulation but have not assigned these effects to specific habenula subnuclei. Here, we have developed a genetic model in which neurons of the dorsal medial habenula (dMHb) are developmentally eliminated, via tissue-specific deletion of the transcription factor Pou4f1 (Brn3a). Mice with dMHb lesions perform poorly in motivation-based locomotor behaviors, such as voluntary wheel running and the accelerating rotarod, but show only minor abnormalities in gait and balance and exhibit normal levels of basal locomotion. These mice also show deficits in sucrose preference, but not in the forced swim test, two measures of depression-related phenotypes in rodents. We have also used Cre recombinase-mediated expression of channelrhodopsin-2 and halorhodopsin to activate dMHb neurons or silence their output in freely moving mice, respectively. Optical activation of the dMHb in vivo supports intracranial self-stimulation, showing that dMHb activity is intrinsically reinforcing, whereas optical silencing of dMHb outputs is aversive. Together, our findings demonstrate that the dMHb is involved in exercise motivation and the regulation of hedonic state, and is part of an intrinsic reinforcement circuit.

  • exercise motivation
  • interpeduncular nucleus
  • intracranial self-stimulation
  • medial habenula
  • optogenetics
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The Journal of Neuroscience: 34 (34)
Journal of Neuroscience
Vol. 34, Issue 34
20 Aug 2014
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Role of the Dorsal Medial Habenula in the Regulation of Voluntary Activity, Motor Function, Hedonic State, and Primary Reinforcement
Yun-Wei A. Hsu, Si D. Wang, Shirong Wang, Glenn Morton, Hatim A. Zariwala, Horacio O. de la Iglesia, Eric E. Turner
Journal of Neuroscience 20 August 2014, 34 (34) 11366-11384; DOI: 10.1523/JNEUROSCI.1861-14.2014

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Role of the Dorsal Medial Habenula in the Regulation of Voluntary Activity, Motor Function, Hedonic State, and Primary Reinforcement
Yun-Wei A. Hsu, Si D. Wang, Shirong Wang, Glenn Morton, Hatim A. Zariwala, Horacio O. de la Iglesia, Eric E. Turner
Journal of Neuroscience 20 August 2014, 34 (34) 11366-11384; DOI: 10.1523/JNEUROSCI.1861-14.2014
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Keywords

  • exercise motivation
  • interpeduncular nucleus
  • intracranial self-stimulation
  • medial habenula
  • optogenetics

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