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Research Articles, Cellular/Molecular

Histamine Release in the Prefrontal Cortex Excites Fast-Spiking Interneurons while GABA Released from the Same Axons Inhibits Pyramidal Cells

Diana Lucaci, Xiao Yu, Paul Chadderton, William Wisden and Stephen G. Brickley
Journal of Neuroscience 11 January 2023, 43 (2) 187-198; DOI: https://doi.org/10.1523/JNEUROSCI.0936-22.2022
Diana Lucaci
1Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
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Xiao Yu
1Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
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Paul Chadderton
2School of Physiology, Pharmacology and Neuroscience, University of Bristol, Bristol, United Kingdom
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William Wisden
1Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
3UK Dementia Research Institute Center at Imperial, Imperial College London, London SW7 2AZ, United Kingdom
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Stephen G. Brickley
1Department of Life Sciences, Imperial College London, London SW7 2AZ, United Kingdom
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Abstract

We studied how histamine and GABA release from axons originating from the hypothalamic tuberomammillary nucleus (TMN) and projecting to the prefrontal cortex (PFC) influence circuit processing. We optostimulated histamine/GABA from genetically defined TMN axons that express the histidine decarboxylase gene (TMNHDC axons). Whole-cell recordings from PFC neurons in layer 2/3 of prelimbic, anterior cingulate, and infralimbic regions were used to monitor excitability before and after optostimulated histamine/GABA release in male and female mice. We found that histamine-GABA release influences the PFC through actions on distinct neuronal types: the histamine stimulates fast-spiking interneurons; and the released GABA enhances tonic (extrasynaptic) inhibition on pyramidal cells (PyrNs). For fast-spiking nonaccommodating interneurons, histamine released from TMNHDC axons induced additive gain changes, which were blocked by histamine H1 and H2 receptor antagonists. The excitability of other fast-spiking interneurons in the PFC was not altered. In contrast, the GABA released from TMNHDC axons predominantly produced divisive gain changes in PyrNs, increasing their resting input conductance, and decreasing the slope of the input–output relationship. This inhibitory effect on PyrNs was not blocked by histamine receptor antagonists but was blocked by GABAA receptor antagonists. Across the adult life span (from 3 to 18 months of age), the GABA released from TMNHDC axons in the PFC inhibited PyrN excitability significantly more in older mice. For individuals who maintain cognitive performance into later life, the increases in TMNHDC GABA modulation of PyrNs during aging could enhance information processing and be an adaptive mechanism to buttress cognition.

SIGNIFICANCE STATEMENT The hypothalamus controls arousal state by releasing chemical neurotransmitters throughout the brain to modulate neuronal excitability. Evidence is emerging that the release of multiple types of neurotransmitters may have opposing actions on neuronal populations in key cortical regions. This study demonstrates for the first time that the neurotransmitters histamine and GABA are released in the prefrontal cortex from axons originating from the tuberomammillary nucleus of the hypothalamus. This work demonstrates how hypothalamic modulation of neuronal excitability is maintained throughout adult life, highlighting an unexpected aspect of the aging process that may help maintain cognitive abilities.

  • GABA
  • histamine
  • hypothalamus
  • prefrontal cortex

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The Journal of Neuroscience: 43 (2)
Journal of Neuroscience
Vol. 43, Issue 2
11 Jan 2023
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Histamine Release in the Prefrontal Cortex Excites Fast-Spiking Interneurons while GABA Released from the Same Axons Inhibits Pyramidal Cells
Diana Lucaci, Xiao Yu, Paul Chadderton, William Wisden, Stephen G. Brickley
Journal of Neuroscience 11 January 2023, 43 (2) 187-198; DOI: 10.1523/JNEUROSCI.0936-22.2022

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Histamine Release in the Prefrontal Cortex Excites Fast-Spiking Interneurons while GABA Released from the Same Axons Inhibits Pyramidal Cells
Diana Lucaci, Xiao Yu, Paul Chadderton, William Wisden, Stephen G. Brickley
Journal of Neuroscience 11 January 2023, 43 (2) 187-198; DOI: 10.1523/JNEUROSCI.0936-22.2022
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Keywords

  • GABA
  • histamine
  • hypothalamus
  • prefrontal cortex

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