The DOI matches its Crossref record; 294 of the 295 references it cites were found in a registry or an index.
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.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Positional cloning of the mouse obese gene and its human homologue
Zhang, Y., Proenca, R., Maffei, M., Barone, M., Leopold, L., & Friedman, J. M. (1994) · Nature · doi:10.1038/372425a0 · Cited by 13,419
Prevalence of Overweight and Obesity in the United States, 1999-2004
Ogden, C. L., Carroll, M. D., Curtin, L. R., McDowell, M. A., Tabak, C. J., & Flegal, K. M. (2006) · JAMA · doi:10.1001/jama.295.13.1549 · Cited by 8,720
Brown Adipose Tissue: Function and Physiological Significance
CANNON, B., & NEDERGAARD, J. (2004) · Physiological Reviews · doi:10.1152/physrev.00015.2003 · Cited by 6,433
Leptin and the regulation of body weight in mammals
Friedman, J. M., & Halaas, J. L. (1998) · Nature · doi:10.1038/27376 · Cited by 5,405
Identification and Importance of Brown Adipose Tissue in Adult Humans
Cypess, A. M., Lehman, S., Williams, G., Tal, I., Rodman, D., Goldfine, A. B., Kuo, F. C., Palmer, E. L., Tseng, Y.-H., Doria, A., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0810780 · Cited by 4,399
Cold-Activated Brown Adipose Tissue in Healthy Men
van Marken Lichtenbelt, W. D., Vanhommerig, J. W., Smulders, N. M., Drossaerts, J. M. A. F. L., Kemerink, G. J., Bouvy, N. D., Schrauwen, P., & Teule, G. J. J. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808718 · Cited by 3,452
Functional Brown Adipose Tissue in Healthy Adults
Virtanen, K. A., Lidell, M. E., Orava, J., Heglind, M., Westergren, R., Niemi, T., Taittonen, M., Laine, J., Savisto, N.-J., Enerbäck, S., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0808949 · Cited by 3,058
Excess Deaths Associated With Underweight, Overweight, and Obesity
Flegal, K. M. (2005) · JAMA · doi:10.1001/jama.293.15.1861 · Cited by 2,811
Fat Mobilization in Adipose Tissue Is Promoted by Adipose Triglyceride Lipase
Zimmermann, R., Bogner‐Strauß, J. G., Haemmerle, G., Schoiswohl, G., Birner‐Gruenberger, R., Riederer, M., Lass, A., Neuberger, G., Eisenhaber, F., Hermetter, A., et al. (2004) · Science · doi:10.1126/science.1100747 · Cited by 2,121
The James-Lange Theory of Emotions: A Critical Examination and an Alternative Theory
Cannon, W. B. (1927) · The American Journal of Psychology · doi:10.2307/1415404 · Cited by 1,899
Flagged first, then by citations
1 of the 295 references couldn’t be matched to a known paper.
Research works printed but not linked: 3
- Gesner C . Medici Tigurini Historiae Animalium Liber I de Quadrupedibusuiuiparis. Froschauer, 1551, pp 840–844.
- Heldmaier G, Klaus S, Wiesinger H, Friedrichs U, Wenzel M . Cold acclimation and thermogenesis. In: Malan A, Canguilhem B (eds). Living in the Cold II. John Libbey Eurotext: Montrouge, France, 1989, pp 347–358.
- Song CK, Smith B, Nguyen N, Bartness TJ . Convergence of Efferent and Afferent Circuits to White Adipose Tissue in Siberian Hamsters. Society for Neuroscience: Neuroscience Meeting Planner Chicago, IL, Online 2009.
Cited by
Sorted by citations
Items 401–456 of 456
Gosselin, C. (2012) · uO Research (University of Ottawa) · doi:10.20381/ruor-5130
Carter, E. A., Hamrahi, V. F., Paul, K. W., Bonab, A. A., Jung, W., Tompkins, R. G., & Fischman, A. J. (2014) · Journal of Burn Care & Research · doi:10.1097/bcr.0000000000000035
Garretson, J. T. (2016) · Digital Archive @ GSU · doi:10.57709/8872423
Nguyen, N. L. T. (2022) · Digital Archive @ GSU · doi:10.57709/10063048
Hyland, L. (2017) · doi:10.22215/etd/2017-12229
“Additionally, locomotor activity changed across time (F(10,220)=3.”
BackgroundO papel da melatonina na regulação do tecido adiposo marrom
Halpern, B. (2018) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.5.2018.tde-31102018-131724
Kushner, R. F., PhD, V. L. M., & FRCPath, S. K. M. F. (2013) · doi:10.1002/9781118643570.ch3
Santacruz-Hidalgo, F., & Viscarra-Sanchez, E. (2019) · Bionatura · doi:10.21931/rb/2019.04.02.11
Direct Effects of Pesticides on Brown Adipose Tissue
Llanos, A. (2018) · MacSphere (McMaster University) · doi:10.71548/23083
Diallo, K., Dussault, S., Noll, C., Lopez, A. F., Rivard, A., Carpentier, A. C., & Lim, G. E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/853184
“…During long-term cold exposure, the sympathetic nervous system releases norepinephrine, which acts as the principal activator of thermogenesis (Bartness et al., 2010; Cannon and Nedergaard, 2004; Fischer et al., 2017; Gabaldon et al., 2003; Landsberg et al., 1984; Thomas and Palmiter, 1997).”
BackgroundNew models of adipogenic differentiation highlight a cellautonomous response to temperature
Veličković, K., Leija, H. A. L., McGinlay, S., Symonds, M. E., & Sottile, V. (2020) · Biocell · doi:10.32604/biocell.2020.012942
“Along with SNS input, the parasympathetic nervous system is involved in the regulation of energy expenditure and energy intake (Bartness et al., 2010), for which two small BAT depots, mediastinal and pericardial, are parasympathetically innervated (Giordano et al., 2004; Schafer et al., 1998).”
BackgroundBrown Adipose Tissue in Obesity and Diabetes
Alcalá, M., Herrero, L., Serra, D., & Viana, M. (2020) · Springer eBooks · doi:10.1007/978-3-030-53370-0_4
Spexin modulates molecular thermogenic profile of adipose tissue and thermoregulatory behaviorsPreprint
Sherman, S. B., Gupta, N. K., Harberson, M. T., Powers, R., Rashleigh, R., Talla, R., Thusu, A., & Hill, J. W. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.10.456868
“135 Spexin reduces thermogenic molecular profile of brown and white adipose tissue 136 Thermogenesis requires sympathetic innervation of iBAT [54, 55], which in turn triggers browning of 137 other adipose tissue depots such as gonadal white adipose tissue [12, 13].”
BackgroundLipid antigens in adipose tissue
van Eijkeren, R. J. (2022) · doi:10.33540/1201
Turcotte, L. P. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.738336375.793580374
Participação da via da PI3K em neurônios SF1 do hipotálamo na homeostase energética
de Jesus, A. A. (2023) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.17.2023.tde-08022024-155611
Investigation and description of the New Brain and New Mind hypotheses
Klinedinst, B. S. (2021) · doi:10.31274/td-20240329-457
Izumi-Mishima, Y., Tsutsumi, R., Shiuchi, T., et al. (2024) · eLife · doi:10.7554/elife.99982.1.sa0
Izumi-Mishima, Y., Tsutsumi, R., Shiuchi, T., et al. (2024) · eLife · doi:10.7554/elife.99982.1.sa2
Edwards, M. M., Nguyen, H. K., Dodson, A. D., Herbertson, A. J., Honeycutt, M. K., Slattery, J. D., Rambousek, J. R., Tsui, E. W., Wolden‐Hanson, T., Wietecha, T., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.12.612710
Piezo2 in sensory neurons influences systemic and adipose tissue metabolismPreprint
Passini, F. S., Bornstein, B., Rubin, S., Kuperman, Y., Krief, S., Masschelein, E., Mehlman, T., Brandis, A. S., Addadi, Y., Shalom, S. H.-O., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.27.624676
Nagagata, B. A., Mandarim‐de‐Lacerda, C. A., & Águila, M. B. (2024) · Cell Biochemistry and Function · doi:10.1002/cbf.70034
“Adipocyte multiloculation increases thermogenic capacity and energy expenditure [46].”
Neuronal Regulation of Thermogenesis and Energy Expenditure in Metabolic Syndrome
Kumar, S., Gawli, C., & Patil, C. R. (2024) · Advances in biochemistry in health and disease · doi:10.1007/978-3-031-75686-3_16
Embryonic macrophages in brown adipose tissue are spatially associated with developing nervesPreprint
Félix, I., Ollikainen, J., Haque, A., Karhula, J., Salmi, M., Jokela, H., & Rantakari, P. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.01.16.632922
Effects of therapeutic factors on brown adipose tissue in order to correct obesity
Kurmaev, D. P., Bulgakova, S. V., Treneva, E. V., & Merzlova, P. Y. (2025) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-228-8-7-27
Wu, R. J., Li, F. F., Wang, S., Jia, J., Cui, X., Huang, Y., Zhang, X., Carrillo, J. A., Ding, Z., Song, J., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.21.660886
Masuda, Y., Kawase, M., Kitano, R., Ohbayashi, K., Yabe‐Wada, T., Inoue, H., Tanida, M., & Iwasaki, Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.11.669026
Brown Adipose Tissue and Skeletal Muscle Coordinately Contribute to Thermogenesis in MicePreprint
Izumi-Mishima, Y., Tsutsumi, R., Shiuchi, T., Fujimoto, S., Taniguchi, M., Sugiuchi, M., Tsutsumi, M., Okamatsu‐Ogura, Y., Yoneshiro, T., Kuroda, M., et al. (2025) · eLife · doi:10.7554/elife.99982.2
Sympathetic signaling directs macrophage efferocytosis in thermogenic adipose tissuePreprint
Meyer, S., Witt, J., Liebold, I., López-López, T., Ehlen, L., Leyk, S., Hiefner, J., Haas, D. T., Schlein, C., Sáez, P. J., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.28.685032
“NE, normally released by sympathetic neurons, is a key mediator of BAT thermogenic activation ( 53 ).”
Neuroendocrine Control of Brown Adipocytes: Functions, Beiging, Whitening and AutophagyPreprint
Winne, C. D., Lopez-Vicchi, F., Boneo, L. E., Ornstein, A. M., Lacau-Mengido, I. M., Sorianello, E. M., & Becu-Villalobos, D. (2021) · Research Square · doi:10.21203/rs.3.rs-472876/v1
Gao, H., Tong, X., Hu, W., Wang, Y., Lee, K., Xu, X., Shi, J., Pei, Z., Lu, W., Chen, Y., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19613824
Disruption of Pre-Bötzinger Complex neuropeptidergic tonality controls fear and metabolic responsePreprint
Shetty, S., Farmanbar, A., Toh, P., Yildiz, R., Jang, Y., Duesman, S. J., Warnock, A., Espinoza, D., Stanley, S., Rajbhandari, P., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.01.01.697304
Sparks, B. B., Lima, A. F. S., Osorio, J. S., & Strieder‐Barboza, C. (2026) · Journal of Dairy Science · doi:10.3168/jds.2025-27515 · Cited by 1
Rouquet, T. (2015) · theses.fr (ABES) · doi:10.70675/680971a6z149ez4296z9c76z5ee9dfd53ce5
Impact of LYL1 deficiency on adipocyte differentiation
Hussain, A. (2015) · theses.fr (ABES) · doi:10.70675/510acdbcz6a62z475ezb193z274bc1a6d27d
Métabolisme redox et plasticité tissulaire des tissus adipeux
Jeanson, Y. (2015) · theses.fr (ABES) · doi:10.70675/0a5580f9z0185z4ab1zba28zb59c62a27680
Gènes cibles des hormones thyroïdiennes, un regard nouveau par le prisme des analyses pangénomiques
Zekri, Y. (2022) · theses.fr (ABES) · doi:10.70675/f8d646ffzf184z40e1z848az174a3d652f5d
Gu, Y., Vidal‐Puig, A., & Xu, Y. (2026) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-026-10037-6
Pardeshi, P. J., Velásquez-Ramírez, D., Salazar-Gil, J. D., Cuellar‐Gaviria, T. Z., Baer, L. A., Higuita‐Castro, N., & Stanford, K. I. (2026) · The FASEB Journal · doi:10.1096/fj.202600635r
From Skin to Brain: Antagonism and Parallelism in the MCH and MSH Systems
Alachkar, A., & Civelli, O. (2026) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.70267
“This upregulates uncoupling protein 1 (UCP1), enabling nonshivering thermogenesis and elevating metabolic rate during the active/light phase [ 93 ].”
Experimental Models for Adipose Tissue Transplantation
Oliinyk, D., & Prantl, L. (2026) · Springer eBooks · doi:10.1007/978-3-032-01711-6_15
Lal, R., Soni, N., Agarwal, K., Kondepudi, K. K., Khare, P., Zimmermann, K., Karbownik‐Lewińska, M., Gesing, A., Aggarwal, V., Chopra, K., et al. (2026) · The FASEB Journal · doi:10.1096/fj.202600519rrrr
Evaluation of high-fat diet-induced metabolic impairments in iBAT lipid metabolism using 1H-MRS
Anantharaj, R., Le, G. T. T., Dharmashekar, C., Leow, M. K., Hu, H. H., Shivamallu, C., Eriksson, J. G., Velan, S. S., Ashokkumar, B., & Yaligar, J. (2026) · Magnetic Resonance Materials in Physics Biology and Medicine · doi:10.1007/s10334-026-01392-1
Feng, T., Cui, Y., Bi, X., Liu, Y., Yang, L., Ouyang, D., Xu, W., Zhao, Y., Xi, Y., Yang, Q., et al. (2026) · Frontiers in Microbiology · doi:10.3389/fmicb.2026.1860759
“Accumulating evidence indicates that micro-biota-derived metabolites can modulate sympathetic nervous system activity (Barrea et al., 2019), which in turn drives β -adrenergic activation in brown and beige adipocytes (Bartness et al., 2010; Yan et al., 2025).”
Targeting the peripheral nervous system in adipose tissue with engineered AAV vectors
Willows, J. W., Lazor, L. M., Gunsch, G., Mishra, G., Villa, A. P., Shay, T. F., Steele, A. D., & Townsend, K. L. (2026) · Cell Reports Methods · doi:10.1016/j.crmeth.2026.101542
“34 The neural innervation of adipose tissue is required to regulate important metabolic processes, including lipolysis, adipogenesis, browning, non-shivering thermogenesis.”
Peripheral Neuropathy in Metabolic Stress
Fu, K., Yang, J. H., & Cao, Y. (2026) · International Journal of Molecular Sciences · doi:10.3390/ijms27167301
Kagawa, S., Tanabe, K., Ogawa, K., Hiromura, M., Sugiyama, M., Amo-Shiinoki, K., Toyama, Y., Fujimori, D., Akashi, H., Yokoyama, M., et al. (2026) · Journal of Pharmacy and Pharmacology · doi:10.1093/jpp/rgag090
Sujan, K. M., Tamakoshi, Y., Seok, B. S., Yang, Z., Xu, S., Elfeky, M., Kato-Suzuki, M., & Okamatsu‐Ogura, Y. (2026) · The Journal of Physiological Sciences · doi:10.1016/j.jphyss.2026.100106
“…and bone morphogenetic protein (BMP) signaling, establish brown adipocyte identity [6 – 8], and extrinsic environmental stimuli, particularly temperature, play a critical role in regulating BAT mass and its functional maturation via stimulation of the sympathetic nervous system (SNS) [6,9,10].”
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
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.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review