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 secretion of catecholamine hormone NE.
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What we talk about when we talk about fat
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Neural innervation of white adipose tissue and the control of lipolysis
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“Because we also have reviewed the SNS innervation of WAT recently and across the years (e.g., Bartness et al., 1993, 2010, 2005; Bartness and Song, 2007a,b), we will make every attempt not to repeat this information, although some reiteration is necessary.”
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“Dynamics of adipose organ composition Innervation and adaptation to temperature changes The adipose organ is innervated (Bartness and Bamshad, 1998; Giordano et al., 2008; Bartness et al., 2010), enabling it to interface with the nervous system and respond to physiological and environmental cues.”
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“BAT is innervated exclusively by the SNS (Bartness et al., 2010).”
BackgroundSensory and sympathetic nervous system control of white adipose tissue lipolysis
Bartness, T. J., Shrestha, Y. B., Vaughan, C. H., Schwartz, G. J., & Song, C. K. (2010) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.08.031 · Cited by 289 · see citing works
Self-citationBrown adipose tissue: physiological function and evolutionary significance
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“…afferent signals to the preoptic area in the hypothalamus (Morrison et al. 2014) and to control regions in the brain stem (Nautiyal et al. 2008; Bartness et al. 2010), leading to the activation of postganglionic sympathetic fibers that release noradrenaline to activate BAT (reviewed by Lowell…”
BackgroundBrown-adipose-tissue macrophages control tissue innervation and homeostatic energy expenditure
Wolf, Y., Boura‐Halfon, S., Cortese, N., Haimon, Z., Shalom, H. S., Kuperman, Y., Kalchenko, V., Brandis, A. S., David, E., Segal-Hayoun, Y., et al. (2017) · Nature Immunology · doi:10.1038/ni.3746 · Cited by 251 · see citing works
“Each murine iBAT lobe displays postganglionic sympathetic innervation 26, as can be visualized in Thy1-YFP animals (Fig.”
Secretin-Activated Brown Fat Mediates Prandial Thermogenesis to Induce Satiation
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GABAergic RIP-Cre Neurons in the Arcuate Nucleus Selectively Regulate Energy Expenditure
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Central Fibroblast Growth Factor 21 Browns White Fat via Sympathetic Action in Male Mice
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Self-citationBrown Adipose Crosstalk in Tissue Plasticity and Human Metabolism
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“BAT also exhibits afferent neurons, which feedback on brain regions controlling sympathetic activation of BAT (97).”
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“Adipose tissue, particularly brown fat, is also extensively innervated with sympathetic fibers that stimulate lipolysis in the setting of fasting, leptin administration, and cold exposure (Bartness et al., 2010a,b; Zeng et al., 2015).”
BackgroundAdipose tissue at single-cell resolution
Maniyadath, B., Zhang, Q., Gupta, R. K., & Mandrup, S. (2023) · Cell Metabolism · doi:10.1016/j.cmet.2023.02.002 · Cited by 207 · see citing works
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Gestational Hypoxia and Developmental Plasticity
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Central Control of Brown Adipose Tissue Thermogenesis
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“Another group of afferents likely to influence BAT thermogenesis (Niijima, 1999) arise from both BAT (Bartness et al., 2010) and white adipose tissue (Song et al.”
BackgroundHypothalamic-autonomic control of energy homeostasis
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Rutin ameliorates obesity through brown fat activation
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“Although we cannot exclude the possibility that rutin regulates whole-body energy metabolism via enhancing BAT metabolic activity through stimulating the sympathetic nervous system (50), the cellular experiments indicated that rutin directly activated BAT oxidation in vitro (Fig.”
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“Finally, FGF 21 can be produced by WAT; and BMP 8 b and FGF 21 can be produced by BAT, after cold activation and promote thermogenesis in a paracrine manner. hydroxylase, the enzyme responsible for the secretion of the catecholamine hormone NE [84].”
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“BAT is innervated by the sympathetic nervous system and the activation of UCP1 is mainly regulated by b3-adrenergic receptors.(128) Rats treated with leptin showed increased oxygen consumption and UCP1 mRNA expression, and this response is elevated after fasting.”
BackgroundUCP1-independent thermogenesis
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Self-citationAdipose tissue: friend or foe?
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Self-citationCentral Nervous System Regulation of Brown Adipose Tissue
Morrison, S. F., & Madden, C. J. (2014) · Comprehensive physiology · doi:10.1002/cphy.c140013 · Cited by 151 · see citing works
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“…outflow from brain to BAT (Bamshad, Song, & Bartness, 1999; Oldfield et al., 2002; Song et al., 2008; Zhang et al., 2011) and destruction of the SNS innervation of BAT blocks or severely diminishes BAT responses to all thermogenic challenges tested to date (for review, see Bartness et al., 2010).”
BackgroundSelf-citationObesity: A neuroimmunometabolic perspective
Larabee, C. M., Neely, O. C., & Domingos, A. I. (2020) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0283-6 · Cited by 123 · see citing works
Central control of thermogenesis
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Sex differences in sympathetic innervation and browning of white adipose tissue of mice
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“While BAT is more densely innervated by peripheral sympathetic nerves than WAT [10, 11], innervation levels of adipose tissues positively correlate with the ability to recruit brown adipocytes in WAT [12].”
BackgroundBellocchio, L., Gómez, E. S., Quarta, C., Metna‐Laurent, M., Cardinal, P., Binder, E., Cannich, A., Delamarre, A., Häring, M., Martín‐Fontecha, M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1218573110 · Cited by 118 · see citing works
“To further confirm the activation of peripheral SNS under our study conditions, we analyzed different biochemical parameters also in the brown adipose tissue (BAT), an organ whose functions are critically under the control of the SNS (37).”
MethodRole of leptin resistance in the development of obesity in older patients
Picard, F., Carter, S., Caron, A., & Richard, D. (2013) · Clinical Interventions in Aging · doi:10.2147/cia.s36367 · Cited by 129 · see citing works
“46 Indeed, it has been shown that intracerebroventricular administration of leptin significantly increases insulin sensitivity, glucose utilization, and glucose uptake in peripheral tissue including BAT.”
InfluentialKolditz, C.-I., & Langin, D. (2010) · Current Opinion in Clinical Nutrition & Metabolic Care · doi:10.1097/mco.0b013e32833bed6a · Cited by 115 · see citing works
The Circadian Clock in the Ventromedial Hypothalamus Controls Cyclic Energy Expenditure
Orozco-Solís, R., Aguilar‐Arnal, L., Murakami, M., Peruquetti, R. L., Ramadori, G., Coppari, R., & Sassone‐Corsi, P. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.02.003 · Cited by 116 · see citing works
“This parallels the notions that the BAT is densely innervated by sympathetic efferents (Bartness et al., 2010) and that the sympathetic system controls circadian peripheral functions, including the cyclic fluctuation of epinephrine(Gamble et al.”
BackgroundBrown Adipose Tissue Has Sympathetic-Sensory Feedback Circuits
Ryu, V., Garretson, J. T., Liu, Y., Vaughan, C. H., & Bartness, T. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.3306-14.2015 · Cited by 113 · see citing works
“By contrast, WAT stores/releases lipid and adipokines and has afferents sensitive to both increases in SNS drive (Bartness et al., 2010a) and to leptin (Murphy et al., 2013), that latter perhaps conveying the amounts of stored lipid via this neural conduit (Bartness et al., 2014).”
BackgroundSelf-citationGLP-1 Influences Food and Drug Reward
Hayes, M. R., & Schmidt, H. D. (2016) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2016.02.005 · Cited by 108 · see citing works
Transcriptional Control of Brown and Beige Fat Development and Function
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“Cold is sensed through the central nervous system, which rapidly elicits sympathetic outflow to brown and white adipose depots (17, 18).”
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Cognitive and autonomic determinants of energy homeostasis in obesity
Richard, D. (2015) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2015.103 · Cited by 109 · see citing works
Hypothalamic control of brown adipose tissue thermogenesis
Labbé, S. M., Caron, A., Lanfray, D., Monge-Roffarello, B., Bartness, T. J., & Richard, D. (2015) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2015.00150 · Cited by 108 · see citing works
“SNS Control of Brown Adipose Tissue BAT thermogenesis is highly dependent on the SNS (Bartness et al., 2010; Bartness and Ryu, 2015).”
BackgroundInfluentialSelf-citationJastroch, M., Giroud, S., Barrett, P., Geiser, F., Heldmaier, G., & Herwig, A. (2016) · Journal of Neuroendocrinology · doi:10.1111/jne.12437 · Cited by 105 · see citing works
“BAT thermogenesis is controlled by dense innervation of sympathetic nerve fibres descending from the central nervous system (92, 93).”
BackgroundVaughan, C. H., & Bartness, T. J. (2012) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00640.2011 · Cited by 103 · see citing works
Self-citationHypothalamus and thermogenesis: Heating the BAT, browning the WAT
Contreras, C., Nogueiras, R., Diéguez, C., Medina‐Gómez, G., & López, M. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.08.002 · Cited by 100 · see citing works
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Traveling from the hypothalamus to the adipose tissue: The thermogenic pathway
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“Furthermore there is evidence for anatomical connection between the PVH and the BAT [4,63,114].”
BackgroundParisi, V., Rengo, G., Filardi, P. P., Pagano, G., Femminella, G. D., Paolillo, S., Petraglia, L., Gambino, G., Caruso, A., Grimaldi, M. G., et al. (2016) · Circulation Research · doi:10.1161/circresaha.115.307765 · Cited by 100 · see citing works
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“Based on the data collected in this study, we propose that BMP7, after binding to its receptor–heterodimer on the cell surface of mature brown adipocytes [1], activates the SMAD and p38-ATF2 signaling pathways [2], followed by increased expression of mitochondrial fatty acid transporter, CPT1 [3], which is further act…”
Understanding the brown adipocyte as a contributor to energy homeostasis
Chechi, K., Carpentier, A. C., & Richard, D. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2013.04.002 · Cited by 99 · see citing works
Purinergic transmission in blood vessels
Ralevic, V., & Dunn, W. R. (2015) · Autonomic Neuroscience · doi:10.1016/j.autneu.2015.04.007 · Cited by 95 · see citing works
“, 2003), or sensory (Bartness and Bamshad, 1998; Bartness et al., 2010) innervation is limited.”
BackgroundBatokines: Mediators of Inter-Tissue Communication (a Mini-Review)
Yang, F. T., & Stanford, K. I. (2022) · Current Obesity Reports · doi:10.1007/s13679-021-00465-7 · Cited by 94 · see citing works
“BAT activation upon cold exposure is due to increased sympathetic outflow of norepinephrine [16] which primarily acts on β3-adrenergic receptors.”
BackgroundMannerås, L., Cajander, S. B., Lönn, M., & Stener‐Victorin, E. (2009) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.90947.2008 · Cited by 94 · see citing works
Regulatory microRNAs in Brown, Brite and White Adipose Tissue
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Functional involvement of β3-adrenergic receptors in melanoma growth and vascularization
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“thermogenesis [19], while subsequently it has been described to play important roles in the pathophysiology of the cardiovascular system [20] and the urinary tract [21, 22].”
BackgroundBrain–gut–adipose-tissue communication pathways at a glance
Yi, C., & Tschöp, M. H. (2012) · Disease Models & Mechanisms · doi:10.1242/dmm.009902 · Cited by 92 · see citing works
“Are there neurochemical characteristics specific to each subtype of preautonomic neuron that enable their connections to peripheral organs or tissues (Bartness et al., 2010a; Oldfield et al., 2007; Oldfield et al., 2002)?”
BackgroundBrown adipose tissue as an anti‐obesity tissue in humans
Chechi, K., Nedergaard, J., & Richard, D. (2013) · Obesity Reviews · doi:10.1111/obr.12116 · Cited by 90 · see citing works
“to interscapular BAT, being the most commonly studied classical BAT depot) are distributed in most brain areas including forebrain, midbrain and brainstem such as the preoptic area, zona incerta, suprachiasmatic nucleus, retrochiasmatic area, dorsomedial hypothalamus, paraventricular hypothalamus, lateral hypothalamus…”
BackgroundPeripheral innervation in the regulation of glucose homeostasis
Lin, E., Scott-Solomon, E., & Kuruvilla, R. (2020) · Trends in Neurosciences · doi:10.1016/j.tins.2020.10.015 · Cited by 76 · see citing works
“Parasympathetic nerves are barely detected in adipose tissue, and their role in adipose functions have been proposed to be minor [68].”
BackgroundNeuropathy and neural plasticity in the subcutaneous white adipose depot
Blaszkiewicz, M., Willows, J. W., Dubois, A. L., Waible, S., DiBello, K., Lyons, L. L., Johnson, C. P., Paradie, E., Banks, N., Motyl, K., et al. (2019) · PLOS ONE · doi:10.1371/journal.pone.0221766 · Cited by 87 · see citing works
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“, 2009) and are controlled by activation of local sympathetic nerve fiber (SNF) activity (Bartness et al., 2010; Chi et al., 2018; Guilherme et al., 2019; Jiang et al., 2017).”
Perivascular Adipose Tissue: the Sixth Man of the Cardiovascular System
Cheng, C. K., Bakar, H. A., Gollasch, M., & Huang, Y. (2018) · Cardiovascular Drugs and Therapy · doi:10.1007/s10557-018-6820-z · Cited by 81 · see citing works
Induction of thermogenic adipocytes: molecular targets and thermogenic small molecules
Song, N.-J., Chang, S., Li, D. Y., Villanueva, C. J., & Park, K. W. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2017.70 · Cited by 80 · see citing works
Adipocyte dedifferentiation in health and diseases
Song, T., & Kuang, S. (2019) · Clinical Science · doi:10.1042/cs20190128 · Cited by 79 · see citing works
Nguyen, N. L. T., Barr, C. L., Ryu, V., Cao, Q., Xue, B., & Bartness, T. J. (2016) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00344.2016 · Cited by 77 · see citing works
“In addition, the SNS outflow to WAT and BAT in Siberian hamsters has been extensively characterized (5, 8) and the SNS innervation of their fat tissues is comparable to other mammals with more similarities than differences in the general pattern (2, 42).”
BackgroundSelf-citationLoss of MyoD Promotes Fate Transdifferentiation of Myoblasts Into Brown Adipocytes
Wang, C., Liu, W., Nie, Y., Qaher, M., Horton, H. E., Yue, F., Asakura, A., & Kuang, S. (2017) · EBioMedicine · doi:10.1016/j.ebiom.2017.01.015 · Cited by 76 · see citing works
“This observation suggests that additional factors, such as Notch signaling and sympathetic innervation (Bartness et al., 2010; Pasut et al., 2016), may be required to induce UCP1 expression in the transdifferentiated MyoD adipocytes.”
BackgroundIntact innervation is essential for diet-induced recruitment of brown adipose tissue
Fischer, A. W., Schlein, C., Cannon, B., Heeren, J., & Nedergaard, J. (2018) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00443.2018 · Cited by 74 · see citing works
Poggioli, R., Ueta, C. B., Drigo, R. A. E., Castillo, M., Fonseca, T. L., & Bianco, A. C. (2013) · Obesity · doi:10.1002/oby.20338 · Cited by 74 · see citing works
“β3-induced acceleration of VO2 reflects the potential for adaptive thermogenesis and is thought to take place predominantly in BAT (13, 32).”
BackgroundPham, T. L., He, J., Kakazu, A. H., Jun, B., Bazan, N. G., & Bazán, H. E. P. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m117.801472 · Cited by 74 · see citing works
“The PEDF-R is enriched in white and brown adipose tissues, which are innervated by sensory calcitonin gene-related peptide (CGRP)- and substance P (SP)-positive nerves (17, 18).”
BackgroundThe Importance of Peripheral Nerves in Adipose Tissue for the Regulation of Energy Balance
Blaszkiewicz, M., Willows, J., Johnson, C. P., & Townsend, K. (2019) · Biology · doi:10.3390/biology8010010 · Cited by 65 · see citing works
Peripheral neuropeptide Y Y1 receptors regulate lipid oxidation and fat accretion
Zhang, L., Macia, L., Turner, N. A., Enriquez, R. F., Riepler, S. J., Nguyen, A., Lin, S., Lee, N. J., Shi, Y. C., Yulyaningsih, E., et al. (2009) · International Journal of Obesity · doi:10.1038/ijo.2009.232 · Cited by 68 · see citing works
Adrenergic regulation of cellular plasticity in brown, beige/brite and white adipose tissues
Ramseyer, V. D., & Granneman, J. G. (2016) · Adipocyte · doi:10.1080/21623945.2016.1145846 · Cited by 67 · see citing works
“sympathetic innervation of both BAT and WAT has been demonstrated consistently by a variety of methods (for review see refs.(14,17)) including immunochemical detection of tyrosine hydroxylase,(22-26) fluorogold retrograde tracing(27) and electrical recording of nerve activity.”
MethodAdler, E. S., Hollis, J. H., Clarke, I. J., Grattan, D. R., & Oldfield, B. J. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2591-12.2012 · Cited by 69 · see citing works
Neuronal systems and circuits involved in the control of food intake and adaptive thermogenesis
Caron, A., & Richard, D. (2016) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13263 · Cited by 68 · see citing works
- 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 › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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