Cited by 679Adipose Tissue and MetabolismPhysiological and biochemical adaptationsRegulation of Appetite and Obesity

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Nonshivering thermogenesis and its adequate measurement in metabolic studies

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Cannon, Barbara, Nedergaard, Jan·2011·Journal of Experimental Biology

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Abstract

Alterations in nonshivering thermogenesis are presently discussed as being both potentially causative of and able to counteract obesity. However, the necessity for mammals to defend their body temperature means that the ambient temperature profoundly affects the outcome and interpretation of metabolic experiments. An adequate understanding and assessment of nonshivering thermogenesis is therefore paramount for metabolic studies. Classical nonshivering thermogenesis is facultative, i.e. it is only activated when an animal acutely requires extra heat (switched on in minutes), and adaptive, i.e. it takes weeks for an increase in capacity to develop. Nonshivering thermogenesis is fully due to brown adipose tissue activity; adaptation corresponds to the recruitment of this tissue. Diet-induced thermogenesis is probably also facultative and adaptive and due to brown adipose tissue activity. Although all mammals respond to injected/infused norepinephrine (noradrenaline) with an increase in metabolism, in non-adapted mammals this increase mainly represents the response of organs not involved in nonshivering thermogenesis; only the increase after adaptation represents nonshivering thermogenesis. Thermogenesis (metabolism) should be expressed per animal, and not per body mass [not even to any power (0.75 or 0.66)]. A 'cold tolerance test' does not examine nonshivering thermogenesis capacity; rather it tests shivering capacity and endurance. For mice, normal animal house temperatures are markedly below thermoneutrality, and the mice therefore have a metabolic rate and food consumption about 1.5 times higher than their intrinsic requirements. Housing and examining mice at normal house temperatures carries a high risk of identifying false positives for intrinsic metabolic changes; in particular, mutations/treatments that affect the animal's insulation (fur, skin) may lead to such problems. Correspondingly, true alterations in intrinsic metabolic rate remain undetected when metabolism is examined at temperatures below thermoneutrality. Thus, experiments with animals kept and examined at thermoneutrality are likely to yield an improved possibility of identifying agents and genes important for human energy balance.

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Background
Sleep Depth Enhancement Through Ambient Temperature Manipulation in Mice
Ajwad, A. A., Huffman, D., Yaghouby, F., OrHara, B. F., & Sunderam, S. (2018) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/embc.2018.8512557 · Cited by 2
“The TNZ is in the neighborhood of 30oC for mice [18,19].”
Background
Argonaute-2 is associated to brown adipose tissue activation
Roger, E., Dumortier, O., Pisani, D. F., Gautier, N., OBBERGHEN, E. V., & Hinault, C. (2019) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2019.05.018 · Cited by 2
Adipose Structure (White, Brown, Beige)
Pellegrinelli, V., Vidal‐Puig, A., & Carobbio, S. (2023) · Springer eBooks · doi:10.1007/978-3-031-40116-9_23 · Cited by 2
Voluntary Wheel Running as an Effective Intervention in the Management of Excessive Food Usage in CD-1 Mice (Mus musculus)
Skurnack, A. M. E., Lane, S. P., Garman, L., Burke, A. L., Williams, W. R., & Budda, M. L. (2024) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-24-040 · Cited by 2
Divergent selection for basal metabolic rate in mice affects the abundance of UCP1 protein: implications for translational studies
Brzęk, P., Selewestruk, P., Sadowska, J., Gębczyński, A. K., Książek, A., Kalinovich, A., Nedergaard, J., & Konarzewski, M. (2024) · The Journal of Physiology · doi:10.1113/jp286669 · Cited by 2
“…that translational experiments in laboratory mice should be carried out at thermoneutrality (usually 30°C) to remove the effect of low ambient temperature on the energy budget and thus make it more comparable to humans (Cannon & Nedergaard, 2011; Ganeshan & Chawla, 2017; Maloney et al., 2014).”
InfluentialSelf-citation
Brown Adipose Tissue, Adiposity, and Menopausal Status in Women at Mid‐Life
Brown, D. E., Shreyer, S., Witkowski, S., & Sievert, L. L. (2025) · American Journal of Biological Anthropology · doi:10.1002/ajpa.70073 · Cited by 2
Personality and metabolic scope in wild mice
Blumberg, W., Fiedler, A., & Careau, V. (2025) · Journal of Experimental Biology · doi:10.1242/jeb.250374 · Cited by 2
“Up to 8 mice could be measured at a time in our custom-built cabinet, which was temperature controlled to be within the thermal neutral zone of the mice (28°C) (Cannon and Nedergaard, 2011).”
Adipose Structure (White, Brown, Beige)
Peirce, V. J., Pellegrinelli, V., & Vidal‐Puig, A. (2015) · Springer eBooks · doi:10.1007/978-3-319-12125-3_23-1 · Cited by 3
Type 2 Immunity and Metabolism
Prahalad, P., Odegaard, J. I., & Chawla, A. (2015) · Springer eBooks · doi:10.1007/978-1-4939-2911-5_9 · Cited by 2
Eosinophils and Type 2 Cytokine Signaling in Macrophages Support the Biogenesis of Cold-induced Beige Fat
Jung, Y. (2016) · Journal of Bacteriology and Virology · doi:10.4167/jbv.2016.46.1.44 · Cited by 2
Sex Differences in Some Physiological Effects of Cold Season or Short-Term Cold Exposure in Adult Albino Rat
Shalaby, A., & Eliwa, K. A. A.-S. (2015) · Endocrinology & Metabolic Syndrome · doi:10.4172/2161-1017.1000159 · Cited by 2
Effects of Nesting Material on the Toxicologic Assessment of Cyclophosphamide in Crl:CD1(ICR) Mice
Brochu, C. P., Winnicker, C. L., Provencher, A., Debien, E., Gariépy, S., & Gaskill, B. N. (2018) · Journal of the American Association for Laboratory Animal Science · doi:10.30802/aalas-jaalas-17-000114 · Cited by 2
Myeloid-resident neuropilin-1 influences brown adipose tissue in obesity
Diaz-Marin, R., Crespo‐Garcia, S., Wilson, A. M., Buscarlet, M., Dejda, A., Fournier, F., Juneau, R., Alquier, T., & Sapieha, P. S. (2021) · Scientific Reports · doi:10.1038/s41598-021-95064-w · Cited by 2
Xiphoid nucleus of the midline thalamus controls cold-induced food seekingPreprint
Lal, N. K., Le, P., Aggarwal, S., Zhang, A., Wang, K., Qi, T., Pang, Z., Yang, D., Nudell, V., Yeo, G. W.-M., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.16.533067 · Cited by 2
Mitochondrial Biogenesis in White Adipose Tissue Mediated by JMJD1A-PGC-1 Axis Limits Age-Related Metabolic DiseasePreprint
Ito, R., Xie, S., Tumenjargal, M., Sugahara, Y., Yang, C., Takahashi, H., Arai, M., Inoue, S., Uchida, A., Nakano, K., et al. (2023) · SSRN Electronic Journal · doi:10.2139/ssrn.4576656 · Cited by 2
Crosstalk between Gut Sensory Ghrelin Signaling and Adipose Tissue Sympathetic Outflow Regulates Metabolic HomeostasisPreprint
Thomas, M. A., Cui, X., Artinian, L. R., Cao, Q., Jing, J., Silva, F. C., Wang, S., Zigman, J. M., Sun, Y., Shi, H., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.25.568689 · Cited by 3
Brown adipose tissue thermogenesis rhythms are driven by the SCN independent of adipocyte clocksPreprint
Paschos, G. K., Lordan, R., Hollingsworth, T., Lekkas, D., Kelch, S., Loro, E., Verginadis, I. I., Khurana, T. S., Sengupta, A., Weljie, A. M., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.10.28.620609 · Cited by 2
An obesogenic diet uncovers disparate changes in uncoupling protein 1 content and lipid synthesis and storage in rat brown adipose tissue
Wright, D. C. (2022) · The Journal of Physiology · doi:10.1113/jp284107 · Cited by 1
“It is activated by the sympathetic nervous system resulting in a UCP1-dependent uncoupling of oxidative phosphorylation from ATP generation leading to the generation of heat (Cannon & Nedergaard, 2011).”
Background
Rearing mice at 22°C programs increased capacity to respond to chronic exposure to cold but not high fat diet
Neri, D., Ramos-Lobo, A. M., Lee, S., Lafond, A., & Zeltser, L. M. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101740 · Cited by 1
“Both involve an initial acute activation phase, called facultative thermogenesis, that evolves into an adaptive phase during chronic exposure [3].”
Background
Adaptive thermogenesis of the brown adipose tissue in Apodemus chevrieri during cold acclimation
Gao, W., & Zhu, W. (2024) · Animal Biology · doi:10.1163/15707563-bja10134 · Cited by 2
Associations of Amino Acids with the Risk of Prediabetes: A Case-Control Study from Kazakhstan
Nurtazina, A., Voitsekhovskiy, I., Kanapiyanov, B., Toishimanov, M., Dautov, D., Karibayev, K., Smail, Y. M., Kozhakhmetova, D. K., & Dyussupov, A. (2024) · Journal of Personalized Medicine · doi:10.3390/jpm14101067 · Cited by 1
“BCAAs play a vital role in the metabolism of brown adipose tissue (BAT) [43].”
Background
The metabolically protective energy expenditure increase of Pik3r1 -related insulin resistance is not explained by Ucp1-mediated thermogenesis
Luijten, I. H. N., Onishi, A., McKay, E. J., Bengtsson, T., & Semple, R. K. (2025) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00449.2024 · Cited by 1
Effects of FGF21, soluble TGFBR2, and environmental temperature on metabolic dysfunction in lipodystrophic mice
Maung, J. N., Chen, Y., Hoose, K. S., Adler, R. E., Hariri, H., Dickson, M. J., Hetrick, T. A., Ferguson, G. A., Schill, R. L., Mori, H., et al. (2025) · JCI Insight · doi:10.1172/jci.insight.194882 · Cited by 1
“Mice undergo nonshivering thermogenesis at standard housing temperatures, resulting in elevated energy expenditure, altered metabolic profiles, and increased food intake and physical activity (28, 29).”
Comparative analysis of naked mole-rat thermogenesis and its potential to maintain euthermia in response to cold
Mikhalchenko, A. E., Corrigan, J. K., He, Y., Péterfi, Z., Yim, S. H., Lee, S., Deng, Z., Amoroso, V. G., Gorbunova, V., Seluanov, A., et al. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2600755123 · Cited by 1
“This revealed the remarkable met abolic plasticity and cold adaptation in this species (28, 45).”
Influential
Long-term exposure to moderate cold reduces incidence of reperfusion tachyarrhythmias in rats
Vebr, P., Galatik, F., Marvanová, A., Elsnicová, B., Hornikova, D., Vecka, M., Spinova, S., Novakova, O., & Zurmanova, J. M. (2025) · Journal of Applied Physiology · doi:10.1152/japplphysiol.00509.2025 · Cited by 1
Deletion of MMP12 improves energy metabolism and brown adipose tissue function in mice prone to cardiometabolic disease
Amor, M., Diaz, M., Fuerlinger, A., Svecla, M., Bianco, V., Schooltink, L., Dobrijević, A., Schwarz, B., Akhmetshina, A., Vujić, N., et al. (2025) · Journal of Lipid Research · doi:10.1016/j.jlr.2025.100951 · Cited by 1
“Although we cannot rule out the that the thermogenic response is primarily driven by muscle shivering rather than by BAT activity (61), our results demonstrate the beneficial effect of MMP12 loss on whole-body and BAT metabolism.”
Retrograde control of sympathetic neuron-satellite glia interactions by target-derived NGF signaling
Kumari, R., Boehm, E. D., Paşcalău, R., Pfeiffer, R. L., Jones, B. W., Tampakakis, E., & Kuruvilla, R. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116697 · Cited by 1
“50 The contact-dependent effects were mediated by PlexinA4 and Sema3a/6a expression in neurons and SGCs, respectively, as well as glial gap junction signaling mediated by Connexin 43.”
Photoperiod-driven browning of white adipose tissue via the calcium signaling pathway in Brandt's voles
Zou, D., Wang, T., Gao, X., Luo, Y., Zhao, Y., Guo, N., & Wang, D. (2026) · Journal of Experimental Biology · doi:10.1242/jeb.252066 · Cited by 1
Sulforaphene‐Enriched Raphanus sativus L. Seed Extract Promotes Norepinephrine‐Induced Thermogenesis and Weight Loss by Modulating the Interplay Between Adipocytes and Immune Cells in Adipose Tissue
Hur, G., Lee, T. K., Kim, J. H., Yang, H., & Lee, K. W. (2026) · Phytotherapy Research · doi:10.1002/ptr.70282 · Cited by 1
“…released from sympathetic nerve fibers in AT, where it binds to beta-adrenergic receptors (ADRB), triggering a signaling cascade that activates uncoupling protein-1 (UCP1) in adipocytes, promoting mitochondrial respiration, metabolic rate, and leading to thermogenesis (Cannon and Nedergaard 2011).”
White adipose atrophy exacerbates cold stress and accelerates aging in male mice
Liu, Z., Hu, W., Tan, X., Sun, S., Huang, X., Meng, Y., Zhao, N., Wang, M., Wu, W., Qian, M., et al. (2026) · Nature Communications · doi:10.1038/s41467-026-71857-3 · Cited by 1
“Impaired thermal insulation in male Lmna f/f ;AC mice Laboratory mice are usually housed at 20 ‒ 24 °C, which is lower than the thermoneutral temperature (30°C), and thus they constantly face chronic innocuous cold stress 23 .”
Thermoneutrality Accelerates a Distinctive Metabolic Dysfunction–Associated Steatohepatitis Phenotype in a Diet-Induced Male Mouse Model With Similarities to Human Disease
Leke, R., Tan, J. Y., Ling, S., Siddiqui, M., Kakol‐Palm, D., Lindblom, A., Andréasson, A., Pellegrini, G., Söderberg, M. P., Zuydam, N. V., et al. (2026) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2026.101866 · Cited by 1
Adrenocortical and bioenergetic responses to cold in laboratory-born northern red-backed voles (Myodes rutilus) from two populations in south Siberia, Russia
Polikarpov, I. A., Titova, T. V., Kondratyuk, E. Y., & Новиков, Е. А. (2018) · Canadian Journal of Zoology · doi:10.1139/cjz-2016-0314 · Cited by 1
Adipose Structure (White, Brown, Beige)
Pellegrinelli, V., Vidal‐Puig, A., & Carobbio, S. (2023) · Springer eBooks · doi:10.1007/978-3-319-12125-3_23-2 · Cited by 1
The maintenance of core temperature in SCUBA divers: Contributions of anthropometrics, patent foramen ovale, and non-shivering thermogenesis
Bradbury, K. E., DiMarco, K. G., Futral, J. E., Lord, R. N., Edward, J. A., Barak, O. F., Glavičić, I., Milos, I., Drviš, I., Dujić, Ž., et al. (2024) · Journal of science and medicine in sport · doi:10.1016/j.jsams.2024.07.010 · Cited by 1
Resting Body Temperature and Long-Term Survival in Older Adults at a Mental Health Center: Cross-Sectional and Longitudinal Data
Chmielewski, P. P., Strzelec, B., Data, K., Chmielowiec, K., Mozdziak, P. E., & Kempisty, B. (2025) · Journal of Clinical Medicine · doi:10.3390/jcm14030713 · Cited by 1
Controlling Thermogenesis: Understanding the Role of PRDM16 in the Development and Function of Brown Fat
Harms, M. (2015) · Scholarly Commons (University of Pennsylvania) · Cited by 1
Effects of Long-Term Food Restriction Under Thermoneutral Conditions on Brown Adipose Tissue of Laboratory Mice
Elsukova, E. I., Mizonova, O. V., & Medvedev, L. N. (2015) · Bulletin of Experimental Biology and Medicine · doi:10.1007/s10517-015-3023-5 · Cited by 1
Sex differences in nonshivering thermogenesis in the wild
Brzęk, P. (2021) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2021.111402 · Cited by 1
“…form 1 July 2021; Accepted 5 July 2021 Molecular and Cellular Endocrinology 536 (2021) 111402 Another reason might be that unambiguous quantification of such a complex trait as NST is difficult to achieve experimentally (Cannon and Nedergaard, 2011; Nedergaard and Cannon, 2013; Trayhurn, 2017).”
Autonomic Nervous System Response to Repeated Cold Exposure
Simmons, J. (2012) · Louisiana State University · doi:10.31390/gradschool_theses.2819 · Cited by 1
“Instead, cellular respiration is used to produce heat instead of fuel (Cannon & Nedergaard, 2011).”
BackgroundMethodInfluential
Les souris comme modèle des maladies humaines : une affaire de température ?
Forest, C. D. (2018) · Ethics Medicine and Public Health · doi:10.1016/j.jemep.2018.05.004 · Cited by 1
Adipocyte-specific deletion of the oxygen-sensor PHD2 sustains elevated energy expenditure at thermoneutralityPreprint
Gomez-Salazar, M. A., Cervera, I. P., Wang, R., French, K. L., García-Martín, R., Blüher, M., Schofield, C. J., Stimson, R. H., Chavakis, T., Gudmundsson, E. F., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.05.425401 · Cited by 1
“This aligns rodent metabolism more closely with that of humans, providing a better preclinical modelling system (5-7, 18-20).”
Background
The obesity-linked human lncRNA AATBC regulates adipocyte plasticity by stimulating mitochondrial dynamics and respirationPreprint
Giroud, M., Kotschi, S., Kwon, Y., Thuc, O. L., Hoffmann, A., Gil‐Lozano, M., Karbiener, M., Higareda‐Almaraz, J. C., Khani, S., Tews, D., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.08.09.455681 · Cited by 1
“30 °C [13], but humans are thermoneutral at much lower temperatures and, therefore, humans only display limited thermogenic activity [14], as their warm environment makes NST obsolete.”
Background
A liver-specific mitochondrial carrier that controls gluconeogenesis and energy expenditurePreprint
Yook, J.-S., Taxin, Z. H., Yuan, B., Oikawa, S., Auger, C., Mutlu, B., Puigserver, P., Hui, S. T., & Kajimura, S. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.12.06.519308 · Cited by 1
“The Journal of biological chemistry 273(38):24754-24759.”
Method

Authors: Cannon, B., & Nedergaard, J.
Affiliations: Stockholm University (SE)
Corresponding author: Cannon, Barbara
ORCID: Cannon, Barbara
Nedergaard, Jan
Venue: Journal of Experimental Biology
Publisher: The Company of Biologists
Published: 2011-01-15
Volume: 214
Issue: 2
Pages: 242-253
ISSN: 0022-0949 (ISSN-L)
1477-9145
DOI: 10.1242/jeb.050989
OpenAlex: W2148400263
Cited by: 677
References: 99
Citations by year: 2026: 20 · 2025: 31 · 2024: 32 · 2023: 45 · 2022: 42 · 2021: 55 · 2020: 53 · 2019: 42 · 2018: 69 · 2017: 48 · 2016: 47 · 2015: 42 · 2014: 48 · 2013: 48 · 2012: 41
FWCI: 3.31
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: other-oa
Locations: Journal of Experimental Biology (publishedVersion, other-oa)
PubMed (publishedVersion)
RVC Research Online (Royal Veterinary College) (submittedVersion, cc-by)
Funders: Vetenskapsrådet
Topics: Health Sciences › Medicine › Physiology (medical) › Adipose Tissue and Metabolism
Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
Keywords: non-shivering thermogenesis, brown adipose tissue, thermoneutrality, ambient temperature, metabolic rate measurement, norepinephrine, shivering, diet-induced thermogenesis, obesity, energy balance, mice, fur insulation
MeSH terms: Acclimatization, Animals, Adipose Tissue, Brown, Cold Temperature, Humans, Norepinephrine, Thermogenesis

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Nonshivering thermogenesis and its adequate measurement in metabolic studies

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