Marco Capogna

Sleep and Serotonin Modulate Paracapsular Nitric Oxide Synthase Expressing Neurons of the Amygdala

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaperJournal articleResearchpeer-review

  • Marco Bocchio, MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, UK; Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.
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  • Simon P Fisher, Department of Physiology, Anatomy and Genetics, University of Oxford , Oxford OX1 3PT, UK.
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  • Gunes Unal, MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, UK; Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.
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  • Tommas J Ellender, MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Oxford OX1 3TH, UK; Department of Pharmacology, University of Oxford, Oxford OX1 3QT, UK.
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  • Vladyslav V Vyazovskiy, Department of Physiology, Anatomy and Genetics, University of Oxford , Oxford OX1 3PT, UK.
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  • Marco Capogna

Unraveling the roles of distinct neuron types is a fundamental challenge to understanding brain function in health and disease. In the amygdala, a brain structure regulating emotional behavior, the diversity of GABAergic neurons has been only partially explored. We report a novel population of GABAergic amygdala neurons expressing high levels of neuronal nitric oxide synthase (nNOS). These cells are predominantly localized along basolateral amygdala (BLA) boundaries. Performing ex vivo patch-clamp recordings from nNOS+ neurons in Nos1-CreER;Ai9 mice, we observed that nNOS+ neurons located along the external capsule display distinctive electrophysiological properties, axonal and dendritic arborization, and connectivity. Examining their c-Fos expression, we found that paracapsular nNOS+ neurons are activated during a period of undisturbed sleep following sleep deprivation, but not during sleep deprivation. Consistently, we found that dorsal raphe serotonin [5-hydroxytryptamine (5-HT)] neurons, which are involved in sleep-wake regulation, innervate nNOS+ neurons. Bath application of 5-HT hyperpolarizes nNOS+ neurons via 5-HT1A receptors. This hyperpolarization produces a reduction in firing rate and, occasionally, a switch from tonic to burst firing mode, thereby contrasting with the classic depolarizing effect of 5-HT on BLA GABAergic cells reported so far. Thus, nNOS+ cells are a distinct cell type of the amygdala that controls the activity of downstream neurons in both amygdaloid and extra-amygdaloid regions in a vigilance state-dependent fashion. Given the strong links among mood, sleep deprivation, and 5-HT, the recruitment of paracapsular nNOS+ neurons following high sleep pressure may represent an important mechanism in emotional regulation.

Original languageEnglish
JournaleNeuro
Volume3
Issue5
DOIs
Publication statusPublished - 9 Nov 2016
Externally publishedYes

    Research areas

  • Amygdala, Animals, Dorsal Raphe Nucleus, GABAergic Neurons, Male, Membrane Potentials, Mice, Inbred C57BL, Mice, Transgenic, Nitric Oxide Synthase Type I, Proto-Oncogene Proteins c-fos, Serotonin, Sleep, Sleep Deprivation, Synapses, Tissue Culture Techniques, Journal Article, Research Support, Non-U.S. Gov't

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ID: 120308143