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Research ArticleResearch Article: New Research, Neuronal Excitability

GAD2 Expression Defines a Class of Excitatory Lateral Habenula Neurons in Mice that Project to the Raphe and Pontine Tegmentum

Lely A. Quina, Andrew Walker, Glenn Morton, Victor Han and Eric. E. Turner
eNeuro 24 April 2020, 7 (3) ENEURO.0527-19.2020; DOI: https://doi.org/10.1523/ENEURO.0527-19.2020
Lely A. Quina
1Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101
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Andrew Walker
1Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101
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Glenn Morton
1Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101
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Victor Han
1Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101
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Eric. E. Turner
1Center for Integrative Brain Research, Seattle Children’s Research Institute, Seattle, WA 98101
2Department of Psychiatry and Behavioral Sciences, University of Washington, Seattle, WA 98195
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Abstract

The lateral habenula (LHb) sends complex projections to several areas of the mesopontine tegmentum, the raphe, and the hypothalamus. However, few markers have been available to distinguish subsets of LHb neurons that may serve these pathways. In order to address this complexity, we examined the mouse and rat LHb for neurons that express the GABA biosynthesis enzymes glutamate decarboxylase 1 (GAD1) and GAD2, and the vesicular GABA transporter (VGAT). The mouse LHb contains a population of neurons that express GAD2, while the rat LHb contains discrete populations of neurons that express GAD1 and VGAT. However, we could not detect single neurons in either species that co-express a GABA synthetic enzyme and VGAT, suggesting that these LHb neurons do not use GABA for conventional synaptic transmission. Instead, all of the neuronal types expressing a GABAergic marker in both species showed co-expression of the glutamate transporter VGluT2. Anterograde tract-tracing of the projections of GAD2-expressing LHb neurons in Gad2Cre mice, combined with retrograde tracing from selected downstream nuclei, show that LHb-GAD2 neurons project selectively to the midline structures in the mesopontine tegmentum, including the median raphe (MnR) and nucleus incertus (NI), and only sparsely innervate the hypothalamus, rostromedial tegmental nucleus (RMTg), and ventral tegmental area (VTA). Postsynaptic recording of LHb-GAD2 neuronal input to tegmental neurons confirms that glutamate, not GABA, is the fast neurotransmitter in this circuit. Thus, GAD2 expression can serve as a marker for functional studies of excitatory neurons serving specific LHb output pathways in mice.

  • GABA
  • glutamate
  • lateral habenula
  • nucleus incertus
  • raphe

Footnotes

  • The authors declare no competing financial interests.

  • This work was supported by National Institutes of Health Grants R01-DA035838 (to E.E.T.) and R01-MN093667 (to E.E.T.).

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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GAD2 Expression Defines a Class of Excitatory Lateral Habenula Neurons in Mice that Project to the Raphe and Pontine Tegmentum
Lely A. Quina, Andrew Walker, Glenn Morton, Victor Han, Eric. E. Turner
eNeuro 24 April 2020, 7 (3) ENEURO.0527-19.2020; DOI: 10.1523/ENEURO.0527-19.2020

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GAD2 Expression Defines a Class of Excitatory Lateral Habenula Neurons in Mice that Project to the Raphe and Pontine Tegmentum
Lely A. Quina, Andrew Walker, Glenn Morton, Victor Han, Eric. E. Turner
eNeuro 24 April 2020, 7 (3) ENEURO.0527-19.2020; DOI: 10.1523/ENEURO.0527-19.2020
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Keywords

  • GABA
  • glutamate
  • lateral habenula
  • nucleus incertus
  • raphe

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