CNS cell groups projecting to sympathetic outflow of tail artery: neural circuits involved in heat loss in the rat
Abstract
In the rat, approximately 20% of total body heat-loss occurs by sympathetically mediated increases in blood flow through an elaborate system of arteriovenous anastomoses in the skin of its tail. In this study, the CNS cell groups that regulate this sympathetic outflow were identified by the viral transneuronal labeling method. Pseudorabies virus was injected into the wall of the ventral tail artery in rats that had their cauda equina transected to eliminate the somatic innervation of the tail. After 4-7 days survival, the pattern of CNS transneuronal labeling was studied. Sympathetic preganglionic neurons in the T11-L2 (mainly L1) levels of the intermediolateral cell column (IML) were labeled by 4 days. After 5 days, sympathetic pre-motor neurons (i.e., supraspinal neurons that project to the IML) were identified near the ventral medullary surface; some of these contained serotonin immunoreactivity. Additional groups of the sympathetic premotor areas were labeled by 6 days post-injection, including the rostral ventrolateral medulla (C1 adrenergic neurons), rostral ventromedial medulla, caudal raphe nuclei (serotonin neurons in the raphe pallidus and magnus nuclei), A5 noradrenergic cell group, lateral hypothalamic area and paraventricular hypothalamic area (oxytocin-immunoreactive neurons). Seven days after the PRV injections, additional cell groups in the telencephalon (viz., bed nucleus of the stria terminalis, medial and lateral preoptic areas and medial preoptic nucleus), diencephalon (viz., subincertal nucleus, zona incerta as well as dorsal, dorsomedial, parafascicular, posterior and ventromedial hypothalamic nuclei) and midbrain (viz., periaqueductal gray matter, precommissural nucleus, Edinger-Westphal nucleus and ventral tegmental area) were labeled. The discussion is focused on the CNS cell groups involved in the control of body temperature and fever.
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In rats, the tail is the primary heat exchange organ.
“In rats, the tail is the primary heat exchange organ. This is due to its extensive vascularization, the presence of arterio-venous anastomoses, lack of fur, and high surface area to volume ratio (Gordon, 1990; Smith et al., 1998).”
From Modulation of body temperature and LH secretion by hypothalamic KNDy (kisspeptin, neurokinin B and dynorphin) neurons: A novel hypothesis on the mechanism of hot flushes (2013) · cites this paper as Smith et al., 1998
Cites
The circadian rhythm of body temperature
Refinetti, R., & Menaker, M. (1992) · Physiology & Behavior · doi:10.1016/0031-9384(92)90188-8 · Cited by 735 · see citing works
Simerly, R. B., & Swanson, L. W. (1988) · The Journal of Comparative Neurology · doi:10.1002/cne.902700205 · Cited by 592 · see citing works
Strack, A. M., Sawyer, W. B., Hughes, J., Platt, K. B., & Loewy, A. D. (1989) · Brain Research · doi:10.1016/0006-8993(89)90098-x · Cited by 591 · see citing works
Self-citationThermal biology of the laboratory rat
Gordon, C. J. (1990) · Physiology & Behavior · doi:10.1016/0031-9384(90)90025-y · Cited by 521 · see citing works
Strack, A. M., Sawyer, W. B., Platt, K. B., & Loewy, A. D. (1989) · Brain Research · doi:10.1016/0006-8993(89)90063-2 · Cited by 489 · see citing works
Self-citationTemperature Receptors in the Central Nervous System
Boulant, J. A., & Dean, J. B. (1986) · Annual Review of Physiology · doi:10.1146/annurev.ph.48.030186.003231 · Cited by 286 · see citing works
Ventromedial Preoptic Prostaglandin E2 Activates Fever-Producing Autonomic Pathways
Scammell, T. E., Elmquist, J. K., Griffin, J. D., & Saper, C. B. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06246.1996 · Cited by 249 · see citing works
Am, S., & Loewy, A. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-07-02139.1990 · Cited by 233 · see citing works
Self-citationSYMPATHETIC ACTIVITY IN MAN AFTER SPINAL CORD INJURY
Stjernberg, L., Blumberg, H., & Wallin, B. G. (1986) · Brain · doi:10.1093/brain/109.4.695 · Cited by 233 · see citing works
THE TAIL OF THE RAT, IN TEMPERATURE REGULATION AND ACCLIMATIZATION
Rand, R. P., Burton, A. C., & Ing, T. (1965) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y65-025 · Cited by 232 · see citing works
Jansen, A. S. P., Wessendorf, M. W., & Loewy, A. D. (1995) · Brain Research · doi:10.1016/0006-8993(95)00276-v · Cited by 229 · see citing works
Self-citationMarson, L., Platt, K. B., & McKenna, K. E. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90471-q · Cited by 190 · see citing works
Haxhiu, M. A., Jansen, A. S. P., Cherniack, N. S., & Loewy, A. D. (1993) · Brain Research · doi:10.1016/0006-8993(93)90435-p · Cited by 172 · see citing works
Self-citationRotto-Percelay, D. M., Wheeler, J., Osorio, F. A., Platt, K. B., & Loewy, A. D. (1992) · Brain Research · doi:10.1016/0006-8993(92)90829-x · Cited by 144 · see citing works
Self-citationEvidence for on–off control of heat dissipation from the tail of the rat
Young, A. A., & Dawson, N. J. (1982) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y82-057 · Cited by 141 · see citing works
SYMPATHETIC ACTIVITY IN MAN AFTER SPINAL CORD INJURY: OUTFLOW TO SKIN BELOW THE LESION
Wallin, B. G., & Stjernberg, L. (1984) · Brain · doi:10.1093/brain/107.1.183 · Cited by 109 · see citing works
Mode of neural control mediating rat tail vasodilation during heating
O'Leary, D. S., Johnson, J. M., & Taylor, W. F. (1985) · Journal of Applied Physiology · doi:10.1152/jappl.1985.59.5.1533 · Cited by 104 · see citing works
CNS regulation of thermogenesis.
Rothwell, N. J. (1994) · PubMed · Cited by 103 · see citing works
Neurovirulence of pseudorabies virus.
Card, J. P., & Enquist, L. W. (1995) · PubMed · Cited by 95 · see citing works
Hyperthermia induces c-fos expression in the preoptic area
Scammell, T. E., Price, K., & Sagar, S. M. (1993) · Brain Research · doi:10.1016/0006-8993(93)91280-6 · Cited by 94 · see citing works
Amir, S. (1990) · Brain Research · doi:10.1016/0006-8993(90)91129-5 · Cited by 88 · see citing works
Thermoregulation and Fever in Normal Persons and in Those With Spinal Cord Injuries
Schmidt, K. D., & CHAN, C. W. (1992) · Mayo Clinic Proceedings · doi:10.1016/s0025-6196(12)60394-2 · Cited by 87 · see citing works
Ultrastructure of the stomatogastric ganglion neuropil of the crab, Cancer borealis
Kilman, V. L., & Marder, E. E. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19961021)374:3 · Cited by 81 · see citing works
Warren, W. S., Champney, T. H., & Cassone, V. M. (1994) · Physiology & Behavior · doi:10.1016/0031-9384(94)90392-1 · Cited by 75 · see citing works
Johnson, C. D., & Gilbey, M. P. (1996) · The Journal of Physiology · doi:10.1113/jphysiol.1996.sp021764 · Cited by 69 · see citing works
Self-citationKovács, G. L., & de Wied, D. (2008) · Neuroendocrinology · doi:10.1159/000123554 · Cited by 64 · see citing works
Sympathetic activity following paraventricular or ventromedial hypothalamic lesions in rats
Sakaguchi, T., Bray, G. A., & Eddlestone, G. (1988) · Brain Research Bulletin · doi:10.1016/0361-9230(88)90135-9 · Cited by 64 · see citing works
Reduced febrile responses to pyrogens after lesions of the hypothalamic paraventricular nucleus
Horn, T. F. W., Wilkinson, M. F., Landgraf, R., & Pittman, Q. J. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.267.1.r323 · Cited by 63 · see citing works
Jansen, A. S. P., & Loewy, A. D. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00506-4 · Cited by 61 · see citing works
Self-citationBody temperature control of rat tail blood flow
Raman, E. R., Roberts, M. F., & Vanhuyse, V. J. (1983) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1983.245.3.r426 · Cited by 60 · see citing works
Responses of patients with high spinal transection to high ambient temperatures.
Randall, W. C., Wurster, R. D., & Lewin, R. (1966) · Journal of Applied Physiology · doi:10.1152/jappl.1966.21.3.985 · Cited by 60 · see citing works
Sympathetic activity recorded from the rat caudal ventral artery in vivo.
Johnson, C. D., & Gilbey, M. P. (1994) · The Journal of Physiology · doi:10.1113/jphysiol.1994.sp020145 · Cited by 58 · see citing works
Self-citationNAYLOR, A. M., Pittman, Q. J., & Veale, W. L. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp017074 · Cited by 55 · see citing works
Sermasi, E., & Coote, J. H. (1994) · Brain Research · doi:10.1016/0006-8993(94)91331-5 · Cited by 51 · see citing works
Loewy, A. D. (1995) · Elsevier eBooks · doi:10.1016/b978-012397570-6/50021-6 · Cited by 50 · see citing works
Self-citationWhy do elephants flap their ears?
Wright, P. G. (1984) · South African Journal of Zoology · doi:10.1080/02541858.1984.11447891 · Cited by 50 · see citing works
Cutaneous arteriovenous anastomoses present in the tail but absent from the ear of the rat.
Rt, G., & Hales (1977) · PubMed · Cited by 48 · see citing works
Transneuronal Tracing with Alpha-herpesviruses
Ugolini, G. (1995) · Elsevier eBooks · doi:10.1016/b978-012397570-6/50019-8 · Cited by 47 · see citing works
Shibata, M., Benzi, R. H., Seydoux, J., & Girardier, L. (1987) · Brain Research · doi:10.1016/0006-8993(87)91671-4 · Cited by 43 · see citing works
Thompson, G. E., & Stevenson, J. A. F. (1965) · Canadian Journal of Physiology and Pharmacology · doi:10.1139/y65-027 · Cited by 34 · see citing works
The antipyretic effects of centrally administered vasopressin at different ambient temperatures
Wilkinson, M. F., & Kasting, N. W. (1987) · Brain Research · doi:10.1016/0006-8993(87)90209-5 · Cited by 33 · see citing works
The influence of the ventrolateral medulla on thermoregulatory circulations in the rat
Key, B. J., & Wigfield, C. C. (1994) · Journal of the Autonomic Nervous System · doi:10.1016/0165-1838(94)90162-7 · Cited by 31 · see citing works
Thermal reflex sweating in normal and paraplegic man
Seckendorf, R., & Randall, W. C. (1961) · Journal of Applied Physiology · doi:10.1152/jappl.1961.16.5.796 · Cited by 27 · see citing works
Key, B. J., & Wigfield, C. C. (1992) · Neuropharmacology · doi:10.1016/0028-3908(92)90032-k · Cited by 24 · see citing works
Circadian thermosensitive characteristics of suprachiasmatic neurons in vitro
Derambure, P., & Boulant, J. A. (1994) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1994.266.6.r1876 · Cited by 24 · see citing works
A critical role for central vasopressin in regulation of fever during bacterial infection
Cridland, R. A., & Kasting, N. W. (1992) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.1992.263.6.r1235 · Cited by 24 · see citing works
Effect of periaqueductal morphine injection on thermal response in rats.
Shen, Z., Yanase, M., Kanosue, K., & NAKAYAMA, T. (1986) · The Japanese Journal of Physiology · doi:10.2170/jjphysiol.36.485 · Cited by 11 · see citing works
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- Authors
- Smith, J. E., Jansen, A. S. P., Gilbey, M. P., & Loewy, A. D.
- Affiliations
- Washington University in St. Louis (US)
- Corresponding author
- Loewy, Arthur D
- ORCID
- Smith, Julia E
- Venue
- Brain Research
- Publisher
- Elsevier BV
- Published
- 1998-03
- Volume
- 786
- Issue
- 1-2
- Pages
- 153-164
- ISSN
- 0006-8993 (ISSN-L)
- OpenAlex
- W1972615540
- Cited by
- 224
- References
- 47
- Citations by year
- 2023: 2 · 2022: 2 · 2021: 5 · 2020: 9 · 2019: 4 · 2018: 5 · 2017: 2 · 2016: 6 · 2015: 13 · 2014: 7 · 2013: 5 · 2012: 5
- FWCI
- 7.15
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Brain Research (publishedVersion)
- PubMed (publishedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Wellcome Trust
- National Heart, Lung, and Blood Institute (HL25449)
- Topics
- Health Sciences › Medicine › Physiology › Thermoregulation and physiological responses
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Keywords
- tail blood flow, sympathetic outflow, heat loss, thermoregulation, fever, intermediolateral cell column, sympathetic premotor neurons, serotonergic neurons, ventrolateral medulla, hypothalamic neurons, oxytocin, bed nucleus of the stria terminalis, preoptic area, medullary blood flow, pseudorabies virus, rats
- MeSH terms
- Animals, Arteries, Body Temperature Regulation, Central Nervous System, Male, Neural Pathways, Synaptic Transmission, Neurons, Sympathetic Nervous System, Tail, Rats, Sprague-Dawley, Rats
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