Elsevier

Neuroscience

Volume 127, Issue 2, 2004, Pages 385-397
Neuroscience

Activation of brain areas in rat following warm and cold ambient exposure

https://doi.org/10.1016/j.neuroscience.2004.05.016Get rights and content

Abstract

Environmental thermal stimuli result in specific and coordinated thermoregulatory response in homeothermic animals. Warm exposure activates numerous brain areas within the cortex, hypothalamus, pons and medulla oblongata. We identified these thermosensitive cell groups in the medulla and pons that were suggested but not outlined by previous physiological studies. Using Fos immunohistochemistry, we localized all the nuclei and cell groups in the rat brain that were activated by warm and cold ambient exposure. These neurons located in the hypothalamus and the brainstem, are part of a network responsible for the thermospecific response elicited by thermal stress. Comparison of the distribution of Fos-immunoreactive cells throughout the rat brain revealed topographical differences between the patterns of activated cells following warm and cold environmental exposure. Among several brain regions, warm exposure elicited c-fos expression specifically in the ventrolateral part of the medial preoptic area, the central subdivision of the lateral parabrachial nucleus and the caudal part of the peritrigeminal nucleus, whereas cold stress resulted in c-fos expression in the ventromedial part of the medial preoptic area, the external subdivision of the lateral parabrachial nucleus and the rostral part of the peritrigeminal nucleus. These neurons are part of a network coordinating specific response to warm or cold exposure. The topographical differences suggest that well-defined cell groups and subdivisions of nuclei are responsible for the specific physiological (endocrine, autonomic and behavioral) changes observed in different thermal environment.

Section snippets

Experimental procedures

Adult male Sprague–Dawley rats (280–320 g) were used according to the requirements of the National Institute of Mental Health Animal Committee (n=36, four of each study group: 30, 60, 120, 180 min warm exposure; 30, 60, 120, 180 min cold exposure and control). All experiments of the present study were conformed to the guidelines and ethical requirements of the Institutional Animal Care and Use Committees and to the guidelines of the National Institute of Mental Health Animal Care. The number of

Results

Short-term warm and cold ambient exposure of the animals elicited rapid activation of a variety of neural cells in the CNS. Fos immunoreactivity detected in brain regions of animals following warm ambient exposure was compared to cold-stressed as well as to control animals. Several regions, like the shell portion of the accumbens nucleus, septohypothalamic nucleus, the rostral part of the medial preoptic area, the supraoptic nucleus, the lateral retrochiasmatic area, the supramamillary nucleus,

Discussion

Thermal exposure is known to elicit a variety of physiological responses (Satinoff, 1978). The neuroanatomical representation of the physiological (autonomic, endocrine, behavioral) reactions can be followed up by histochemical techniques. The c-fos proto-oncogene was found to be expressed following neuronal activity (Morgan and Curran, 1991); therefore, the distribution of Fos-positive neurons reflects the activated brain areas in response to stress.

Warm environmental exposure resulted in

Acknowledgements

We would like to thank Mrs. Judit Helfferich and Dr. Éva Mezey for their help in immunohistochemical techniques and Mr. Ricardo Dreyfuss for the exceptional photography. This work was supported by grant from the Hungarian National Science Foundation, OTKA TS040771.

References (47)

  • H. Sato

    Raphe-spinal and subcoeruleo-spinal modulation of temperature signal transmission in rats

    J Therm Biol

    (1993)
  • T.E. Scammell et al.

    Hyperthermia induces c-fos expression in the preoptic area

    Brain Res

    (1993)
  • M. Szekely

    The vagus nerve in thermoregulation and energy metabolism

    Auton Neurosci

    (2000)
  • R. Szymusiak et al.

    Acute thermoregulatory effects of unilateral electrolytic lesions of the medial and lateral preoptic area in rats

    Physiol Behav

    (1982)
  • L. Zaborszky et al.

    Cholecystokinin innervation of the ventral striatumA morphological and radioimmunological study

    Neuroscience

    (1985)
  • L. Amini-Sereshki et al.

    Brain stem tonic inhibition of thermoregulation in the rat

    Am J Physiol

    (1984)
  • S. Arancibia et al.

    Neuroendocrine and autonomous mechanisms underlying thermoregulation in cold environment

    Neuroendocrinology

    (1996)
  • J. Baffi et al.

    Fine topography of brain areas activated by cold stress

    Neuroendocrinology

    (2000)
  • J. Bligh

    The thermosensitivity of the hypothalamus and thermoregulation in mammals

    Biol Rev Camb Philos Soc

    (1966)
  • J.A. Boulant et al.

    The effect of spinal and skin temperatures on the firing rate and thermosensitivity of preoptic neurons

    J Physiol

    (1974)
  • J.A. Boulant et al.

    Responses of thermosensitive preoptic and septal neurons to hippocampal and brain stem stimulation

    J Neurophysiol

    (1977)
  • J.A. Boulant

    Hypothalamic mechanisms of thermoregulation

    Fed Proc

    (1981)
  • J.A. Boulant et al.

    Temperature receptors in the central nervous system

    Annu Rev Physiol

    (1986)
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