Reassessing the Role of Histaminergic Tuberomammillary Neurons in Arousal Control
Open accessAbstract
The histaminergic neurons of the tuberomammillary nucleus (TMN HDC ) of the posterior hypothalamus have long been implicated in promoting arousal. More recently, a role for GABAergic signaling by the TMN HDC neurons in arousal control has been proposed. Here, we investigated the effects of selective chronic disruption of GABA synthesis (via genetic deletion of the GABA synthesis enzyme, glutamic acid decarboxylase 67) or GABAergic transmission (via genetic deletion of the vesicular GABA transporter (VGAT)) in the TMN HDC neurons on sleep–wake in male mice. We also examined the effects of acute chemogenetic activation and optogenetic inhibition of TMN HDC neurons upon arousal in male mice. Unexpectedly, we found that neither disruption of GABA synthesis nor GABAergic transmission altered hourly sleep–wake quantities, perhaps because very few TMN HDC neurons coexpressed VGAT. Acute chemogenetic activation of TMN HDC neurons did not increase arousal levels above baseline but did enhance vigilance when the mice were exposed to a behavioral cage change challenge. Similarly, acute optogenetic inhibition had little effect upon baseline levels of arousal. In conclusion, we could not identify a role for GABA release by TMN HDC neurons in arousal control. Further, if TMN HDC neurons do release GABA, the mechanism by which they do so remains unclear. Our findings support the view that TMN HDC neurons may be important for enhancing arousal under certain conditions, such as exposure to a novel environment, but play only a minor role in behavioral and EEG arousal under baseline conditions. SIGNIFICANCE STATEMENT The histaminergic neurons of the tuberomammillary nucleus of the hypothalamus (TMN HDC ) have long been thought to promote arousal. Additionally, TMN HDC neurons may counter-regulate the wake-promoting effects of histamine through co-release of the inhibitory neurotransmitter, GABA. Here, we show that impairing GABA signaling from TMN HDC neurons does not impact sleep–wake amounts and that few TMN HDC neurons contain the vesicular GABA transporter, which is presumably required to release GABA. We further show that acute activation or inhibition of TMN HDC neurons has limited effects upon baseline arousal levels and that activation enhances vigilance during a behavioral challenge. Counter to general belief, our findings support the view that TMN HDC neurons are neither necessary nor sufficient for the initiation and maintenance of arousal under baseline conditions.
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These observations are consistent with recent reports that TMN histaminergic neurons do not simply encode baseline arousal.
“These observations are consistent with recent reports that TMN histaminergic neurons do not simply encode baseline arousal.”
From Infraslow histaminergic dynamics govern priming states to gate moment-to-moment memory accessibility (2026) · cites this paper as [35]
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McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0011
A theory of the septo-hippocampal system (SHS)
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0010
Symptoms and syndromes of anxiety
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0013
The neurology of anxiety—survival circuits
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0002
The treatment of anxiety and fear disorders
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0014
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0011
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0015
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0009
The anxiolytic drugs—our key tool
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0003
List of online appendices and reviews
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0010
A conceptual theory of the goal inhibition system
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.003.0005
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0006
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0004
McNaughton, N., & Gray, J. A. (2024) · Oxford University Press eBooks · doi:10.1093/oso/9780198843313.002.0005
The neurotransmitters of sleep and arousal
Fan, C. (2024) · Theoretical and Natural Science · doi:10.54254/2753-8818/37/20240186
Shao, F.-B., Fang, J.-F., Wang, S.-S., Qiu, M., Danning, X., Jin, X., Liu, J., Shao, X., Shen, Z., Liang, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16607063
Shao, F.-B., Fang, J.-F., Wang, S.-S., Qiu, M., Danning, X., Jin, X., Liu, J., Shao, X., Shen, Z., Liang, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16607057
Shao, F.-B., Fang, J.-F., Wang, S.-S., Qiu, M., Danning, X., Jin, X., Liu, J., Shao, X., Shen, Z., Liang, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16607060
Shao, F.-B., Fang, J.-F., Wang, S.-S., Qiu, M., Danning, X., Jin, X., Liu, J., Shao, X., Shen, Z., Liang, Y., et al. (2021) · Figshare · doi:10.6084/m9.figshare.16607066
Giannoni, P. (2025) · The Receptors · doi:10.1007/978-3-031-98921-6_6
Meckes, A. J., & Meckes, J. W. (2026) · Frontiers in Sleep · doi:10.3389/frsle.2025.1736866
Ma, Z., Cao, W., Zhang, J. Y., & 洪宗元 (2026) · Neuroreport · doi:10.1097/wnr.0000000000002276
Broadhurst, R. Y., Voltarelli, V. A., Weber, J., Gallo, D. J., Meehan, W. P., III, de Souza, R. W. A., Otterbein, L. E., & Fuller, P. M. (2026) · Neurochemistry International · doi:10.1016/j.neuint.2026.106212
Self-citationThe influence of histamine and antihistamines on microglial regulation and neuroinflammation
Pehar, M., Westhoff, J., Fischer, D., & Kulka, M. (2026) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/cjpp-2025-0317
Thermoregulatory roles of preoptic area histamine H 1 receptor-expressing neuronsPreprint
Piñol, R. A., Valeri, A., Xiao, C., Hadley, C., Goldschmidt, A. I., Kerspern, D., Kulkarni, S., Gavrilova, O., Lutas, A., Krashes, M. J., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.09.22.753241
- Authors
- Venner, A., Mochizuki, T., De Luca, R., Anaclet, C., Scammell, T. E., Saper, C. B., Arrigoni, E., & Fuller, P. M.
- Affiliations
- Beth Israel Deaconess Medical Center (US)
- University of Toyama (JP)
- University of Massachusetts Chan Medical School (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2019-09-23
- Volume
- 39
- Issue
- 45
- Pages
- 8929-8939
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6832676
- OpenAlex
- W2976060716
- Cited by
- 70
- References
- 44
- Citations by year
- 2026: 6 · 2025: 1 · 2024: 28 · 2023: 4 · 2022: 8 · 2021: 15 · 2020: 7 · 2019: 1
- FWCI
- 4.50
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- The Journal of the American Medical Association (JAMA) Network (American Medical Association) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-sa)
- Funders
- National Heart, Lung, and Blood Institute (P01HL095491)
- National Institute of Neurological Disorders and Stroke (R01NS092652, R01NS085477, R01NS103161, R01NS073613)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Sleep and Wakefulness Research
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Keywords
- tuberomammillary nucleus, histaminergic neurons, arousal control, GABAergic neurotransmission, vesicular GABA transporter, glutamic acid decarboxylase 67, sleep-wake regulation, sustained attention, chemogenetic activation, optogenetic inhibition
- MeSH terms
- Action Potentials, Animals, Arousal, gamma-Aminobutyric Acid, Glutamate Decarboxylase, Histamine, Hypothalamic Area, Lateral, Male, Mice, Inbred C57BL, Neurons, Sleep, Vesicular Inhibitory Amino Acid Transport Proteins, Mice
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