Warm sensitive neurons of the preoptic area regulate ambient temperature related changes in sleep in the rat

Indian Journal of Physiology and Pharmacology

Volumn 55, Issue 3, 2011, Pages 262-271

  Kumar, Deependra ^a,b   Kumar, Velayudhan Mohan ^a,b   Mallick, Hruda Nanda ^a  

^a ALL INDIA INSTITUTE OF MEDICAL SCIENCES   (India)

^b SREE CHITRA TIRUNAL INSTITUTE FOR MEDICAL SCIENCES AND TECHNOLOGY   (India)

Author keywords

Capsaicin warm sensitive neurons ambient temperature sleep body temperature preoptic area thermal preference

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BODY TEMPERATURE MEASUREMENT; BRAIN NERVE CELL; CELL DESTRUCTION; CONTROLLED STUDY; ENVIRONMENTAL TEMPERATURE; HEAT SENSITIVITY; MALE; NONHUMAN; PREOPTIC AREA; RAT; REM SLEEP; SLEEP PATTERN; SLEEP QUALITY; SLEEP STAGE; SLEEP TIME; SLEEP WAKING CYCLE; SLOW WAVE SLEEP; THERMORECEPTOR; THERMOREGULATION; TRANSITION TEMPERATURE; WARMING;

ANIMALS; BODY TEMPERATURE REGULATION; CAPSAICIN; MALE; PREOPTIC AREA; RATS; RATS, WISTAR; SLEEP;

EID: 84857300262     PISSN: 00195499     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (62)

1. Teague RS, Ranson SW. The role of the anterior hypothalamus in temperature regulation. Am J Physiol 1936; 117: 562-570.
2. Lipton JM. Effects of preoptic lesion on heat escape responding and colonic temperature in the rat. Physiol Behav 1968; 3: 165-169.
3. Boulant JA. Hypothalamic mechanisms in thermoregulation. Fed Proc 1981; 40: 2843-2850.
4. Satinoff E, Liran J, Clapman R. Aberrations of circadian body temperature rhythms in rats with medial preoptic lesions. Am J Physiol 1982; 242: R352-R357.
5. Szymusiak R, Satinoff E. Acute thermoregulatory effects of unilateral electrolytic lesions of the medial and lateral preoptic area in rats. Physiol Behav 1982; 28: 161-170.
6. Datta S, Kumar VM, Chhina GS, Singh B. Tonic activity of medial preoptic norepinephrine mechanism for body temperature maintenance in sleeping and awake rats. Brain Res Bull 1985; 15: 447-451.
7. Datta S, Kumar VM, Chhina GS, Singh B. Effect of application of serotonin in medial preoptic area on body temperature and sleep-wakefulness. Indian J Exp Biol 1987; 25: 681-685.
8. Szymusiak R, Danowski J, McGinty D. Exposure to heat restores sleep in cats with preoptic/ anterior hypothalamic cell loss. Brain Res 1991; 541: 134-138.
9. John J, Kumar VM. Effect of NMDA lesion of the medial preoptic neurons on sleep and other functions. Sleep 1998; 21: 587-598.
10. Kumar VM, Khan NA. Role of the preoptic neurons in thermoregulation in rats. Arch Clin Exp Med 1998; 7: 24-27.
11. Pal R, Mallick HN, Kumar VM. Role of catecholaminergic terminals in the preoptic area in behavioral thermoregulation in rats. Indian J Physiol Pharmacol 2002; 46: 434-440.
12. Glotzbach SF, Heller HC. Changes in the thermal characteristics of hypothalamic neurons during sleep and wakefulness. Brain Res 1984; 309: 17-26.
13. McGinty D, Szymusiak R. Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep. Trends Neurosci 1990; 13: 480-487.
14. Osaka T, Matsumura H. Noradrenergic inputs to sleep-related neurons in the preoptic area from the locus coeruleus and the ventrolateral medulla in the rat. Neurosci Res 1994; 19: 39-50.
15. Talwar A, Kumar VM. Effect of carbachol injection in the mPOA on sleep-wakefulness and body temperature in free moving rats. Indian J Physiol Pharmacol 1994; 38: 163-168.
16. Osaka T, Matsumura H. Noradrenaline inhibits preoptic sleep active neurons through alpha-2 receptors in the rat. Neurosci Res 1995; 21: 323-330.
17. Alam MN, McGinty D, Szymusiak R. Neuronal discharge of preoptic/anterior hypothalamic thermosensitive neurons: relation to NREM sleep. Am J Physiol 1995; 269: R1240-R1249.
18. Ramesh V, Kumar VM. The role of alpha-2 receptors in the medial preoptic area in the regulation of sleep-wakefulness and body temperature. Neuroscience 1998; 85: 807-817.
19. Vetrivelan RA, Mallick HN, Kumar VM. Changes in body temperature and sleep-wakefulness after intrapreoptic injection of methoxamine in rats. Neural Plast 2003; 10: 267-278.
20. Vetrivelan R, Mallick HN, Kumar VM. Sleep induction and temperature lowering by medial preoptic alpha(1) adrenergic receptors. Physiol Behav 2006; 87: 707-713.
21. Srividya R, Mallick HN, Kumar VM. Differences in the effects of medial and lateral preoptic lesions on thermoregulation and sleep in rats. Neuroscience 2006; 139: 853-864.
22. Kumar VM, Vetrivelan R, Mallick HN. Noradrenergic afferents and receptors in the medial preoptic area: neuroanatomical and neurochemical links between the regulation of sleep and body temperature. Neurochem Int 2007; 50: 783-790.
23. Schmidek WR, Hoshimo K, Schmidek M, Timo-Iaria C. Influence of environmental temperature on the sleep-wakefulness cycle in the rat. Physiol Behav 1972; 8: 363-371.
24. Sakaguchi S, Glotzbach SF, Heller HC. Influence of hypothalamic and ambient temperatures on sleep in kangaroo rats. Am J Physiol 1979; 237: R80-R88.
25. Szymusiak R, Satinoff E. Maximal REM sleep time defines a narrower thermoneutral zone than does minimal metabolic rate. Physiol Behav 1981; 26: 687-690.
26. Thomas TC, Kumar VM. Effect of ambient temperature on sleep-wakefulness in normal and medial preoptic area lesioned rats. Sleep Res Online 2000; 3: 141-145.
27. Gulia KK, Mallick HN, Kumar VM. Ambient temperature related sleep changes in rats neonatally treated with capsaicin. Physiol Behav 2005; 85: 414-418.
28. Kumar D, Mallick HN, Kumar VM. Ambient temperature induces maximum sleep in rats. Physiol Behav 2009; 98: 186-191.
29. Mahapatra AP, Mallick HN, Kumar VM. Changes in sleep on chronic exposure to warm and cold ambient temperatures. Physiol Behav 84: 287-294. Erratum in: Physiol Behav 2005; 85: 517-518.
30. Alföldi P, Rubicsek G, Cserni G, Obál F Jr. Brain and core temperatures and peripheral vasomotion during sleep and wakefulness at various ambient temperatures in the rat. Pflugers Arch 1990; 417: 336-341.
31. Wünnenberg W, Brück K. Studies on the ascending pathways from the thermosensitive region of the spinal cord. Pflugers Arch 1970; 321: 233-241.
32. Simon E, Iriki M. Ascending neurons highly sensitive to variations of spinal cord temperature. J Physiol (Paris) 1971; 63: 415-417.
33. Simon E. Temperature signals from skin and spinal cord converging on spinothalamic neurons. Pflugers Arch 1972; 337: 323-332.
34. Boulant JA. Hypothalamic control of thermoregulation: neurophysiological basis. In: Morgane PJ, Panksepp J, eds. Handboook of the Hypothalamus. New York: Dekker 1980; 1-82.
35. Obál F Jr, Tobler I, Borbély AA. Effect of ambient temperature on 24 hour sleep-wake cycle in normal and capsaicin treated rats. Physiol Behav 1983; 30: 425-430.
36. Sterman MB, Clemente CD. Forebrain inhibitory mechanisms: sleep patterns induced by basalforebrain stimulation in the behaving cat. Exp Neurol 1962; 6: 103-117.
37. Hellstrom B, Hammel HT. Some characteristics of temperature regulation in the unanesthetized dog. Am J Physiol 1967; 213: 547-556.
38. Roberts WW, Robinson TC. Relaxation and sleep induced by warming of the preoptic region and anterior hypothalamus in cats. Exp Neurol 1969; 25: 282-294.
39. Roberts WW, Mooney RD. Brain areas controlling thermoregulatory grooming, prone extension, locomotion and tail vasodilatation in rats. J Comp Physiol Psychol 1974; 86: 470-480.
40. Hammel HT, Jacobson DC, Stolwijk JA, Hardy JD, Stromme SB. Temperature regulation by hypothalamic proportional control with an adjustable set point. J Appl Physiol 1963; 18: 1146-1154.
41. Ray B, Mallick HN, Kumar VM. Changes in thermal preference, sleep-wakefulness, body temperature and locomotor activity of rats during continuous recording for 24-hours. Behav Brain Res 2004; 154: 519-526.
42. Ray B, Mallick HN, Kumar VM. Changes in sleep-wakefulness in the medial preoptic area lesioned rats: role of thermal preference. Behav Brain Res 2005; 158: 43-52.
43. Jancsó-Gábor A, Szolcsányi J, Jancsó N. Stimulation and desensitization of the hypothalamic heat-sensitive structures by capsaicin in rats. J Physiol 1970; 208: 449-459.
44. Szolcsányi J. Capsaicin type pungent agents producing pyrexia. In: Milton AS, eds. Handbook of Experimental Pharmacology. Berlin, Springer-Verlag 1982; 437-478.
45. Hajós M, Obál F Jr, Jancsó G, Obál F. The capsaicin sensitivity of the preoptic region is preserved in adult rats pretreated as neonates, but lost in rats pretreated as adults. Naunyn Schmiedebergs Arch Pharmacol 1983; 324: 219-222.
46. Szolcsányi J, Joo F, Jancsó-Gábor A. Mitochondrial changes in preoptic neurons after capsaicin desensitization of the hypothalamic thermodetectors in rats. Nature 1971; 229: 116-117.
47. Jancsô G, Wollemann M. The effect of capsaicin on the adenylate cyclase activity of rat brain. Brain Res 1977; 123: 323-329.
48. Hajós M, Obál F Jr, Jancsó G, Obál F. Capsaicin impairs preoptic serotonin-sensitive structures mediating hypothermia in rats. Neurosci Lett. 1985; 54: 97-102.
49. Hori T, Shibata M, Kiyohara T, Nakashima T, Asami A. Responses of anterior hypothalamicpreoptic thermosensitive neurons to locally applied capsaicin. Neuropharmacology 1988; 27: 135-142.
50. Kumar VM, Datta S, Chinna GS, Gandhi N, Singh B. Sleep-awake responses elicited from medial preoptic area on application of norepinephrine and phenoxybenzamine in free moving rats. Brain Res 1984; 322: 322-325.
51. DeGroot J. The rat forebrain in stereotaxic coordinates. Verh Konink Nederland Akad Wetenschap Natuurkunde. 1959; 52: 1-40.
52. Jancsó N, Jancsó-Gábor A, Szolcsányi J. Direct evidence for neurogenic inflammation and its prevention by denervation and by pretreatment with capsaicin. Br J Pharmacol Chemother 1967; 31: 138-151.
53. John J, Kumar VM, Gopinath G, Ramesh V, Mallick H. Changes in sleep-wakefulness after kainic acid lesion of the preoptic area in rats. Jpn J Physiol 1994; 44: 231-242.
54. Srividya R, Mallick HN, Kumar VM. The medial septum acts through the medial preoptic area for thermoregulation and works with it for sleep regulation. Indian J Physiol Pharmacol 2007; 51: 261-273.
55. Boulant JA, Dean JB. Temperature receptors in the central nervous system. Ann Rev Physiol 1986; 48: 639-654.
56. Nauta WJH. Hypothalamic regulation of sleep in rats: An experimental study. J Neurophysiol 1946; 9: 285-316.
57. John J, Kumar VM, Gopinath G. Recovery of sleep after fetal preoptic transplantation in medial preoptic area-lesioned rats. Sleep 1998; 21: 601-606.
58. Van Someren EJW. Sleep propensity is modulated by circadian and behavior-induced changes in cutaneous temperature. J Therm Biol 2004; 29: 437-444.
59. Grahn DA, Radeke CM, Heller HC. Arousal state vs. temperature effects on neuronal activity in subcoeruleus area. Am J Physiol 1989; 256: R840-R849.
60. Cevolani D, Parmeggiani PL. Responses of extrahypothalamic neurons to short temperature transients during the ultradian wake-sleep cycle. Brain Res Bull 1995; 37: 227-232.
61. Alam MN, McGinty D, Szymusiak R. Thermosensitive neurons of the diagonal band in rats: relation to wakefulness and non-rapid eye movement sleep. Brain Res 1997; 752: 81-89.
62. Kumar VM. Sleep is neither a passive nor an active phenomenon. Sleep Biol Rhythms 2010; 8: (in press).