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Sympathetic and sensory innervation of brown adipose tissue
Open accessAbstract
The innervation of brown adipose tissue (BAT) by the sympathetic nervous system (SNS) is incontrovertible and, with its activation, functions as the principal, if not exclusive, stimulator of BAT thermogenesis. The parasympathetic innervation of BAT only appears in two minor BAT depots, but not in the major interscapular BAT (IBAT) depot. BAT thermogenesis is triggered by the release of norepinephrine from its sympathetic nerve terminals, stimulating β3-adrenoceptors that turns on a cascade of intracellular events ending in activation of uncoupling protein-1 (UCP-1). BAT also has sensory innervation that may function to monitor BAT lipolysis, a response necessary for activation of UCP-1 by fatty acids, or perhaps responding in a feedback manner to BAT temperature changes. The central sympathetic outflow circuits ultimately terminating in BAT have been revealed by injecting the retrograde viral transneuronal tract tracer, pseudorabies virus, into the tissue; moreover, there is a high degree of colocalization of melanocortin 4-receptor mRNA on these neurons across the neural axis. The necessary and sufficient central BAT SNS outflow sites that are activated by various thermogenic stimuli are not precisely known. In a chronic decerebration procedure, IBAT UCP-1 gene expression can be triggered by fourth ventricular injections of melanotan II, the melanocortin 3/4 receptor agonist, suggesting that there is sufficient hindbrain neural circuitry to generate thermogenic responses with this stimulation. The recent recognition of BAT in normal adult humans suggests a potential target for stimulation of energy expenditure by BAT to help mitigate increased body fat storage.
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“These nerves express tyrosine hydroxylase, the enzyme responsible for the secretion of the catecholamine hormone NE 84.”
From Inter‐organ communication: a gatekeeper for metabolic health (2019) · cites this paper as [84]
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“78 Moreover, an altered sympathetic tone has been hypothesized as a possible cause for the decrease in BAT recruitment in aging.”
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“It was previously known that the adipose tissue responds to physiological and environmental stimuli, due to its high density in nerve fibers in contact with adipocytes, allowing it to interfere with the nervous system [16].”
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“vascularized, as well as innervated by sympathetic nerves, both of which are important factors in regulating thermogenesis [7].”
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“It has been postulated that sensory nerves in BAT serve to sense its thermal status, blood flow, or intracellular lipolytic products and hence regulate its thermogenic activity via the SNS loop (10, 133).”
BackgroundMethodFlett, S., Garcia, J. L., & Cowley, K. C. (2022) · Journal of Neurophysiology · doi:10.1152/jn.00205.2022 · Cited by 39
Foster, M. T., Song, C. K., & Bartness, T. J. (2009) · Obesity · doi:10.1038/oby.2009.345 · Cited by 39
Self-citationDouris, N., Desai, B. N., Fisher, F. M., Cisu, T., Fowler, A. J., Zarebidaki, E., Nguyen, N. L. T., Morgan, D. A., Bartness, T. J., Rahmouni, K., et al. (2017) · Molecular Metabolism · doi:10.1016/j.molmet.2017.05.017 · Cited by 39
“As it is known that both metabolic rate and the BAT thermogenic program are regulated by the SNS [9], we hypothesized that the SNS may play a role in the adaptation to ketogenic diets.”
BackgroundSelf-citationInterplay between the brain and adipose tissue: a metabolic conversation
Díaz‐Castro, F., Morselli, E., & Claret, M. (2024) · EMBO Reports · doi:10.1038/s44319-024-00321-4 · Cited by 44
“These receptors are abundantly expressed in BAT and play crucial roles in adaptive thermogenesis (Bartness et al, 2010), and their sensitivity is controlled, among other factors, by thyroid hormones.”
Osaki, A., Shimizu, H., Ishizuka, N., Suzuki, Y., Mori, M., & Inoue, S. (2012) · Neuroscience Letters · doi:10.1016/j.neulet.2012.05.056 · Cited by 38
Shrestha, Y. B., Vaughan, C. H., Smith, B. J., Song, C. K., Baro, D. J., & Bartness, T. J. (2010) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00535.2009 · Cited by 40
Self-citationSzentirmai, É., & Kapás, L. (2013) · European Journal of Neuroscience · doi:10.1111/ejn.12463 · Cited by 36
“Second, there is extensive afferent innervation arising from the iBAT and reaching the hypothalamic paraventricular nucleus, periaqueductal gray, olivary areas, parabrachial nuclei, raphe nuclei and reticular areas (Bartness et al., 2010; Vaughan & Bartness, 2012).”
BackgroundRepeated weight cycling in obese mice causes increased appetite and glucose intolerance
Simonds, S. E., Pryor, J. T., & Cowley, M. A. (2018) · Physiology & Behavior · doi:10.1016/j.physbeh.2018.05.026 · Cited by 38
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Metabolic signals in sleep regulation: recent insights
Basheer, R., & Shukla, C. (2016) · Nature and Science of Sleep · doi:10.2147/nss.s62365 · Cited by 44
“101,102 There is evidence to suggest that these innervations are temperature sensitive and prevent excessive heating of the tissue by a negative feedback loop.”
Transient receptor potential (TRP) channels: a metabolic TR(i)P to obesity prevention and therapy
Bishnoi, M., Khare, P., Brown, L., & Panchal, S. K. (2018) · Obesity Reviews · doi:10.1111/obr.12703 · Cited by 37
BMP4 facilitates beige fat biogenesis via regulating adipose tissue macrophages
Qian, S., Wu, M., Wang, Y., Zhao, Y., Zou, Y., Pan, J., Tang, Y., Liu, Y., Guo, L., & Tang, Q. (2018) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjy011 · Cited by 35
The Central Clock Neurons Regulate Lipid Storage in Drosophila
DiAngelo, J. R., Erion, R., Crocker, A. J., & Sehgal, A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019921 · Cited by 35
Stress Stimulates Production of Catecholamines in Rat Adipocytes
Květňanský, R., Ukropec, J., Lauková, M., MANZ, B., Pacák, K., & Vargovič, P. (2012) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-012-9822-6 · Cited by 35
“Stress-induced increase in CA levels stimulates fat cell b1, b2, b3 and a2- adrenergic receptors, which activate or inhibit lipolysis (Berlan and Lafontan 1982; Lafontan and Berlan 1995; Lafontan and Langin 2009; Bartness et al. 2010; Giordano et al. 2005).”
BackgroundInfluentialAnsari, A., Bose, S., Yadav, M., Wang, J., Song, Y.-K., Ko, S., & Kim, H. (2016) · Molecules · doi:10.3390/molecules21111522 · Cited by 36
“The hypothalamus is central in the mechanistic chain of the brain-gut-adipose tissue axis because it consists of receptors for neuropeptides as well as adipose tissue-derived adipokines, which ultimately communicate with the brain via neuronal inputs [22].”
BackgroundSacramento, J. F., Martins, F. O., Rodrigues, T., Matafome, P. N., Ribeiro, M. J., Olea, E., & Conde, S. V. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2020.00262 · Cited by 34
“The innervation of the brown adipose tissue by the sympathetic nervous system function as the principal stimulator of brown adipose tissue thermogenesis, being the activation of the sympathetic nervous system known also as one of themain triggers for the browning/beiging of the white adipose tissue (42).”
BackgroundRegulation of thermogenic adipocytes during fasting and cold
Reinisch, I., Schreiber, R., & Prokesch, A. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110869 · Cited by 36
Ferreira, J. M. B. B., Mady, C., Ianni, B. M., Lopes, H. F., Ramires, F. J. A., Salemi, V. M. C., Grupi, C., HACHUL, D. T., & Fernandes, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131447 · Cited by 33
Adipocyte Gs but not Gi signaling regulates whole-body glucose homeostasis
Caron, A., Reynolds, R. P., Castorena, C. M., Michael, N. J., Lee, C. E., Lee, S., Berdeaux, R., Scherer, P. E., & Elmquist, J. K. (2019) · Molecular Metabolism · doi:10.1016/j.molmet.2019.06.019 · Cited by 34
“A prevalent model predicts that activation of adipose b-adrenergic receptors promotes a molecular cascade that triggers the accumulation of cAMP, which results in protein kinase A (PKA) activation [16,17].”
BackgroundTissue-Specific Role of Macrophages in Noninfectious Inflammatory Disorders
Skuratovskaia, D., Vulf, M. A., Хазиахматова, О. Г., Malashchenko, V. V., Komar, A., Shunkin, E. O., Shupletsova, V. V., Гончаров, А. Г., Urazova, O. I., & Litvinova, L. S. (2020) · Biomedicines · doi:10.3390/biomedicines8100400 · Cited by 34
Regulation of Energy Balance and Body Weight by the Brain: A Distributed System Prone to Disruption
Faulconbridge, L. F., & Hayes, M. R. (2011) · Psychiatric Clinics of North America · doi:10.1016/j.psc.2011.08.008 · Cited by 34
Of mice and men: novel insights regarding constitutive and recruitable brown adipocytes
Townsend, K. L., & Tseng, Y.-H. (2015) · International Journal of Obesity Supplements · doi:10.1038/ijosup.2015.5 · Cited by 32
Human torpor: translating insights from nature into manned deep space expedition
Shi, Z., Qin, M., Huang, L., Xu, T., Chen, Y., Hu, Q., Peng, S., Peng, Z., Qu, L., Chen, S., et al. (2020) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12671 · Cited by 31
Carter, E. A., Bonab, A. A., Hamrahi, V. F., Pitman, J. T., Winter, D. G., Macintosh, L. J., Cyr, E. M., Paul, K. W., Yerxa, J., Jung, W., et al. (2011) · Life Sciences · doi:10.1016/j.lfs.2011.04.014 · Cited by 31
“The mechanism(s) for activation of BAT thermogenesis are assumed to be through the sympathetic nervous system (Bartness et al. 2010).”
BackgroundEffect of Thyroid Hormones on Adipose Tissue Flexibility
Volke, L., & Krause, K. (2020) · European Thyroid Journal · doi:10.1159/000508483 · Cited by 35
Thermogenic adipose tissue in energy regulation and metabolic health
Xue, S., Lee, D. P. H., & Berry, D. C. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1150059 · Cited by 31
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Orexin modulation of adipose tissue
Perez‐Leighton, C. E., Billington, C. J., & Kotz, C. M. (2013) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2013.06.007 · Cited by 35
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The “Skinny” on brown fat, obesity, and bone
Devlin, M. J. (2014) · American Journal of Physical Anthropology · doi:10.1002/ajpa.22661 · Cited by 33
“BAT depots respond rapidly to sympathetic activation, thanks to extensive vascularization and sympathetic innervation (Aherne and Hull, 1966; Symonds and Lomax, 1992; Bartness et al., 2010).”
BackgroundTapping into 5-HT3 Receptors to Modify Metabolic and Immune Responses
Irving, H. R., Turek, I., Kettle, C., & Yaakob, N. S. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111910 · Cited by 31
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“Nerve fibers containing NE innervate brown adipose tissue (BAT).(18) Norepinephrine acting on b3-adrenoreceptor is most studied for BAT metabolism and enhances glucose uptake in BAT in vivo.”
BackgroundExercise‐Induced cytokines, diet, and inflammation and their role in adipose tissue metabolism
Al‐Ibraheem, A. M. T., Hameed, A. A. Z., Marsool, M. D. M., Jain, H., Prajjwal, P., Khazmi, I., Nazzal, R., Al-Najati, H. M. H., Al‐Zuhairi, B. H. Y. K., Razzaq, M., et al. (2024) · Health Science Reports · doi:10.1002/hsr2.70034 · Cited by 33
“95 It is found that mice with lower levels of β AR experienced a decrease in metabolic rate and showed a tendency towards obesity.”
BackgroundGlycerolipid Cycling in Thermogenesis, Energy Homeostasis, Signaling, and Diseases
Poursharifi, P., Madiraju, S. R. M., Oppong, A. K., Kajimura, S., Nolan, C. J., Blondin, D. P., & Prentki, M. (2025) · Physiological Reviews · doi:10.1152/physrev.00024.2024 · Cited by 29
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Metadata
- Authors
- Bartness, T. J., Vaughan, C. H., & Song, C. K.
- Affiliations
- Georgia State University (US)
- Corresponding author
- Bartness, T J
- ORCID
- Bartness, T J
- Venue
- International Journal of Obesity
- Published
- 2010-10
- Volume
- 34
- Issue
- S1
- Pages
- S36-S42
- ISSN
- 0307-0565 (ISSN-L)
- 1476-5497
- PMC
- PMC3999344
- OpenAlex
- W1991845771
- Cited by
- 459
- References
- 295
- Citations by year
- 2026: 17 · 2025: 20 · 2024: 29 · 2023: 32 · 2022: 29 · 2021: 22 · 2020: 35 · 2019: 28 · 2018: 25 · 2017: 33 · 2016: 29 · 2015: 26 · 2014: 18 · 2013: 29 · 2012: 41
- FWCI
- 2.86
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- International Journal of Obesity (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Diabetes and Digestive and Kidney Diseases (R37DK35254, R37DK035254)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Lipid metabolism and biosynthesis
- Keywords
- brown adipose tissue, sympathetic innervation, parasympathetic innervation, thermogenesis, norepinephrine, beta3-adrenergic receptor, UCP1, sensory innervation, melanocortin-4 receptor, melanotan II, energy expenditure, pseudorabies virus tracing
- MeSH terms
- Uncoupling Protein 1, Animals, Adipose Tissue, Brown, Humans, Ion Channels, Sympathetic Nervous System, Thermogenesis, Mitochondrial Proteins
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