- Introduction
-
- Many Authors have reported changes in brain
temperature during the ultradian sleep cycle in
several mammalian species. The temperature
decrease in NREM sleep is not discussed here
since it is a normal effect of thermoregulation
operating at a lower set point temperature than
in wakefulness. In contrast, the increase in
brain temperature related to REM sleep appears
paradoxical from the viewpoint of normal
thermoregulation. The problem of the physiologic
mechanisms underlying this temperature change
remains unresolved (cf. 26).
-
- Changes in brain temperature are in general
relevant to both the energy metabolism of the
brain and the function of the
preoptic-hypothalamic thermostat. However, the
increase in temperature related to REM sleep,
amounting to a few tenths of a degree Celsius at
most, may appear of little physiologic
importance from a physicochemical viewpoint (Q
10 effect). Whereas this assertion applies to
neurons lacking high specific thermosensitivity,
a different problem is whether such temperature
change is a feedback signal for specific
thermoresponsive neurons. However, the issue may
be resolved considering the depression in the
responsiveness of the preoptic-hypothalamic
thermostat during REM sleep (cf. 26, 39).
Notwithstanding this conclusion, a review of
experimental results will show that it is
physiologically relevant to appreciate the
mechanisms underlying the brain temperature rise
related to REM sleep.
-
- Physiologic mechanisms for brain
cooling
-
- Brain temperature changes are quantitatively
expressed as the ratio between the changes in
heat content and mass of the nervous tissue
multiplied by its specific heat (AT = AQ/mc).
Heat is produced by cellular energy metabolism
and is transferred to the arterial blood in
inverse relation to its temperature, which is
lower than that of the brain in normal
conditions (25). It is obvious that brain
homeothermy is altered essentially by
quantitative imbalances between metabolic heat
production and heat loss.
-
- There are different mechanisms for cooling
the brain in mammals and more than a single
mechanism may be operative. In general, the cool
venous blood flowing from the systemic heat
exchangers of the body (upper airway mucosa, ear
pinna, horn, tail, skin, according to species)
to the heart mixes with the warm venous blood
returning to the heart from heat-producing body
tissues. This systemic mechanism cools the
arterial blood including that flowing to the
brain (systemic brain cooling). In addition to
systemic brain cooling, there is also a
mechanism for selective brain cooling. In
species like the cat, dog, sheep and goat (23,
25), the carotid blood supply to the brain is
again thermally conditioned prior to entering
into the circle of Willis by countercurrent heat
exchange between carotid rete and venous sinuses
(e.g., sinus cavernosus). The carotid rete is a
network of fine vessels (rudimental in the dog),
derived from the external branch of the common
carotid artery. The arterial blood flowing to
the brain in the carotid rete is surrounded by
sinus venous blood cooled in the upper airway
mucosa and flowing in an opposite direction to
the heart (5, 6, 18, 25). The carotid rete is
connected to the circle of Willis through a
short artery (homologous to the distal part of
the internal carotid artery of species lacking
the carotid rete). As a result of the
countercurrent heat exchange, the temperature of
the carotid blood reaching the circle of Willis
is further decreased with respect to that of the
aortic arch blood (5, 6, 25). Vertebral artery
blood is not thermally conditioned by a
countercurrent heat exchange mechanism and
enters into the circle of Willis at the
temperature of the blood in the aortic arch
(25). In conclusion, the difference between the
temperatures of vertebral artery blood (systemic
cooling only) and carotid artery blood (both
systemic and selective cooling) flowing into the
circle of Willis depends on the heat loss from
the carotid rete. Eventually, the average brain
temperature is determined by the relative
amounts of carotid and vertebral artery blood
contributing to the total blood flow of the
brain.
-
- Another mechanism for selective brain
cooling is typical of species lacking the
carotid rete (e.g., rabbit and rat). It is
provided by conductive heat exchange between the
basal portion of the brain, including the circle
of Willis, and the basal venous sinuses that
drain cool venous blood from the upper airway
mucosa (13).
-
- The effects of systemic and selective brain
cooling appear in the temperatures of the
hindbrain and forebrain, respectively. This is
shown by the positive difference between pontine
and preoptic-hypothalamic temperatures in cats
(4, 41), rabbits (41, 42) and rats (11,
41).
-
- Heat loss from systemic heat exchangers,
affecting carotid blood temperature through the
systemic venous return to the heart (systemic
brain cooling), is the most important
determinant of brain temperature in primates
(24, 25). Concerning humans, in particular,
there is no consensus as to whether a mechanism
for selective brain cooling plays a significant
role (8, 9, 10, 28, 29, 35).
-
- REM sleep related changes in brain
temperature
-
- REM sleep in several mammalian species is
characterized by a rise in brain temperature
(1,3,5,6, 15, 17, 19, 23, 25, 27, 31-33,
40,44,51,56-60). It is remarkable that such rise
occurs at ambient temperatures not only above or
within the ambient thermoneutral zone of the
species but also below this zone (2,
21,40,44-46). In contrast, studies in primates
showed a decrease in hypothalamic temperature
(24, 25) and cortical temperature (47, 54) in
relation to REM sleep at ambient temperatures
close to or within the ambient thermoneutral
zone of the species.
-
- Concerning REM sleep in the two species (cat
and rabbit) considered in detail here, the
increase in brain temperature is related to
systemic heat exchanger vasomotion that is
opposite to that normally observed during NREM
sleep under the influence of the same high or
low ambient temperature. The proximate causes of
such vasomotion are imbalances between
transmural pressure and smooth muscle tonus
during REM sleep, that appear paradoxical from
the thennoregulatory viewpoint (12, 14, 21, 37,
40, 44). The REM sleep related increase in brain
temperature at high ambient temperature appears,
nevertheless, as a consistent result of the
paradoxical replacement of thermoregulatory
vasodilatation in NREM sleep by vasoconstriction
reducing systemic heat loss in REM sleep. In
contrast, the REM sleep related increase in
brain temperature at low ambient temperature
appears clearly inconsistent with the
paradoxical replacement of thermoregulatory
vasoconstriction in NREM sleep by vasodilatation
increasing systemic heat loss in REM sleep.
-
- Mechanisms underlying the REM sleep
related increase in brain temperature
-
- From different viewpoints, many studies
contributed to the early detection of factors
directly underlying the REM sleep related
increase in brain temperature (cf. 36). In
particular, an increase in the metabolic heat
production of the nervous tissue was proposed by
several authors (15, 31, 32, 51, 56). Other
authors proposed the arterial blood flow as a
main factor (17, 30, 48, 49, 54-56), whereas
others considered the arterial blood temperature
the main factor (5, 6, 25).
-
- The metabolic heat production of the nervous
tissue appears an unlikely candidate as the
primary cause of the observed change in brain
temperature. In fact, several studies suggest
that both brain metabolic rate and arterial
blood flow increase in REM sleep with respect to
NREM sleep (cf. 20, 34). On this basis, the
increase in brain metabolic heat production is
indirectly related to the rise in heat clearance
by the increase in arterial blood flow.
Therefore, temperature alone is not a reliable
indicator of changes in metabolic heat
production (cf. 25, 52, 53). In any case,
metabolic heat production is unlikely to play a
major role in the increase of brain temperature
related to REM sleep particularly on the basis
of subsequent experimental evidence.
-
- The other factors at issue are the flow and
temperature of the arterial blood supplied to
the circle of Willis by different sources.
-
- The effects of the transient fall in common
carotid blood flow were studied in cats and
rabbits (4, 38, 42). The fall was provoked by
short (ˆ 100 s) bilateral common carotid
artery occlusion during wakefulness and NREM
sleep at ambient temperature (25 ± 2
°C) close to thermal neutrality. A decrease
in ear pinna temperature and an increase in both
preoptic-hypothalamic and pontine temperatures
were elicited by this procedure. Different
mechanisms underlie these temperature changes.
The short latency and the steepness of the
initial rise in preoptic-hypothalamic
temperature appear as an obvious effect of brain
autoregulation of flow for the following reason.
In response to the metabolic demand of the
cerebral bed, suddenly raised by the fall in the
carotid artery share of cerebral blood flow,
autoregulation (cf. 7) buffers the fall in
carotid blood supply by increasing the supply of
vertebral artery blood. The flow increase in
vertebral artery blood, warmer (systemic cooling
only) than carotid artery blood (both systemic
and selective cooling), initially contributes
more to the increase in preoptic-hypothalamic
temperature than the depression of selective
brain cooling. This temperature approaches but
does not reach the also rising value of the
pontine temperature during the short duration of
bilateral common carotid artery occlusion. The
pontine temperature rises with a lesser slope
than preoptic-hypothalamic temperature as it is
driven by the increasing temperature of
vertebral artery blood. The latter rise is a
result of the decrease in common carotid artery
blood flow depressing systemic heat loss from
upper airway mucosa and ear pinna. Moreover, the
degree of this effect depends also on the
surface area of the ear pinna, since the pontine
temperature increases more slowly and less in
cats than in rabbits (4, 42). In support of the
importance of autoregulation of blood flow, it
is worth mentioning that electroencephalographic
signs of ischemia are absent during bilateral
common carotid artery occlusion of long (up to
300s) but evidently harmless duration in cats
(4). In this case, the preoptic-hypothalamic and
pontine temperatures tend to a plateau following
the initial rise. This is a sign of the new
thermal equilibrium existing between metabolic
heat production and decreased systemic and
selective heat loss. In conclusion, changes in
metabolic heat production are not necessarily
involved in these experimentally induced
temperature changes during wakefulness and NREM
sleep.
-
- Additional experimental evidence shows that
the previous argument also applies to the
spontaneous increase in preoptic-hypothalamic
and pontine temperatures related to REM sleep
(4, 38, 42). This increase is characterized
initially by a rather steep slope from the level
attained at the end of NREM sleep and
subsequently by a plateau. The temperature
plateau lasts for the duration of the REM sleep
episode and shows opposite variations to those
of ear pinna temperature, that is systemic heat
loss.
-
- Bilateral short (ˆ 100 s) occlusion of
the common carotid artery at REM sleep onset in
cats and rabbits does not affect or only
scarcely enhances the spontaneous decrease in
ear pinna temperature and the spontaneous
increase in both preoptichypothalamic and
pontine temperatures. This is a crucial result
showing that common carotid blood flow is
spontaneously decreased on REM sleep occurrence.
Such decrease may be considered the trigger of
an autoregulatory response increasing brain
blood flow in REM sleep. There is experimental
evidence in the cat that the increase in
hypothalamic blood flow during REM sleep is
preceded by an initial transient decrease (16,
50). On this basis, the conclusion is warranted
that bilateral occlusion of common carotid
artery in wakefulness and NREM sleep mimics a
hemodynamic condition occurring spontaneously in
REM sleep. In contrast, short bilateral common
carotid artery occlusion after the end of REM
sleep stops both the spontaneous increase in ear
pinna temperature and the spontaneous decrease
in pontine and preoptic-hypothalamic
temperatures. This shows that common carotid
artery blood flow spontaneously increases after
the end of REM sleep: the increase enhances both
systemic and selective brain cooling in turn
whereas vertebral artery blood flow decreases.
The indirect experimental evidence of a
spontaneous fall and rise in common carotid
artery blood flow during and after REM sleep,
respectively, has recently been confirmed by
direct measurement of this flow in rabbits
(43).
-
- As mentioned before, preoptic-hypothalamic
temperature rises during REM sleep also at low
ambient temperature (2, 21, 40, 44-46). The
event is fairly inconsistent with the actual
increased heat loss due to paradoxical
vasodilatation of the systemic heat exchangers
of the head (ear pinna, upper airway mucosa).
This fact adds further indirect evidence that
autoregulation of brain blood flow in REM sleep
counterbalances the decrease in carotid blood
supply by the increase in vertebral blood supply
that is warmer than the former.
-
- The described hemodynamic mechanisms apply
not only to cats and rabbits but probably also
to rats that show comparable REM sleep related
changes of upper airway mucosa,
preoptic-hypothalamic and pontine temperatures
(11, 12). On the other hand, the remarkable
morphofunctional prevalence of the internal
carotid arteries over the vertebral arteries in
primates (18) underlies unfavorable hemodynamic
conditions, particularly in humans (22), for a
significant enhancement of the blood supply of
the vertebral arteries to the brain during REM
sleep. Although the lack of adequate
experimental evidence precludes any definitive
conclusion, it is probable that brain
temperature changes in primates depend only on
changes in systemic brain cooling during REM
sleep.
-
- Functional implications
-
- The inference of cerebral autoregulation of
vertebral blood flow drawn from the previous
experimental results is fundamental to explain
in detail the mechanism underlying the REM sleep
related rise in preoptic-hypothalamic
temperature in cats and rabbits. However, it
should not be overlooked that the decrease in
common carotid artery blood flow, characterizing
REM sleep (43), reveals a systemic hemodynamic
depression that appears so conspicuous as to
negatively affect also vertebral artery blood
flow and consequently cerebral autoregulation.
In contrast to this inference, an increase in
cerebral blood flow during REM sleep with
respect to NREM sleep was observed in several
species including the cat and rabbit (cf. 20,
34). Therefore, a basic question is how to
reconcile the systemic hemodynamic depression in
REM sleep with thé autoregulatory
increase in cerebral blood flow. This is
conceptually possible considering the factors
that may contribute to an adequate
autoregulation of cerebral blood flow in spite
of systemic unfavorable hemodynamic
circumstances. The anatomical data (cf. 18)
point to important morphosfunctional differences
between the carotid and vertebral tributaries of
the circle of Willis in the species considered
(e.g., complex network of fine vessels of the
carotid rete in the cat; vertebral arteries
larger than internal carotid arteries in the
rabbit). On this basis, higher inflow impedance
for the carotid blood supply than for the
vertebral blood supply to the circle of Willis
is likely in both cats and rabbits. In this
respect, the disappearance of the negative
hydrostatic load as result of the lowered head
posture, and a decrease in cerebral vascular
impedance in relation with cortical activation
in REM sleep also deserve consideration. The
existence of conditions enhancing the vertebral
blood supply to the brain in the rabbit during
REM sleep is also shown by the fact that
arterial blood flow increases more in the
hindbrain than in the forebrain (cf. 20).
-
- The autoregulatory response to the decreased
common carotid artery blood supply to the
forebrain is a result of the alteration of
homeostatic cardiovascular regulation during REM
sleep (cf. 37). However, an additional
autoregulatory increase in vertebral blood
supply is likely to occur as a response to brain
activation in REM sleep with respect to NREM
sleep. The former autoregulatory response is the
most variable, since the "steal" of common
carotid artery blood is due to autonomic events
that are intrinsically irregular. The latter
autoregulatory response is the most stable as
the expression of actual flow-metabolism
coupling due to the stereotyped pattern of brain
activation in REM sleep. Eventually, the overall
temporal coupling of flow and metabolism in the
brain is less consistent in REM sleep than in
both wakefulness and NREM sleep, according to
the different time courses of randomly
interacting peripheral and central physiological
processes during REM sleep.
-
- Conclusion
-
- Summing up, three main factors have been
considered as possibly underlying the brain
temperature rise related to REM sleep: namely,
changes in 1°) the metabolic heat
production of the nervous tissue, 2°) the
arterial blood flow, 3°) the arterial blood
temperature. The present discussion points out
that the first factor is practically not
relevant to the problem. The experimental
evidence supports the view that the proximate
causes of the rise in brain temperature related
to REM sleep are the quantitative shift from
carotid blood supply to vertebral blood supply
to the circle of Willis and the depression of
systemic and selective brain cooling. A remote
cause of the rise in brain temperature is the
systemic hemodynamic alteration in REM sleep.
The instability of autonomic cardiovascular
regulation brings about a "steal" of common
carotid artery blood supplying the brain and the
systemic heat exchangers of the head. A "steal",
depressing both systemic and selective brain
cooling, to be counterbalanced in the species
considered by blood flowing to the brain
primarily from the vertebral arteries.
-
- Summary
-
- The roles of metabolic heat production,
arterial blood flow and temperature in the
genesis of the brain temperature increase
related to REM sleep occurrence in several
mammalian species are discussed on the basis of
available experimental evidence.
-
- The experimental data show that only changes
in arterial blood flow and temperature
consistently underlie the rise in brain
temperature in presence (cat) or absence
(rabbit) of the carotid rete. The alteration of
cardiovascular regulation in REM sleep is the
remote cause of such rise. The proximate causes
are decrease in carotid blood supply and
increase in vertebral blood supply to the brain
and related depression of systemic and selective
brain cooling.
-
- References
-
- I. ADAMS, T. Hypothalamic temperature in the
cat during feeding and sleep. Science, 139:
609-610, 1963.
-
- 2. ALFOLDI, P., RUBICSEK, G., CSERNI, G. AND
OBAL, JR. F. Brain and core temperatures arid
peripheral vasomotion during sleep and
wakefulness at various ambient temperatures in
the rat. Pfluigers Arch., 417: 336-341,
1990.
-
- 3. ALLISON, T. AND VAN TWYVER, H. Sleep in
the moles, Scalopus aquaticus and Condylura
cristata. Exp. Neurol., 27: 564-578, 1970.
-
- 4. AZZAR0NI, A. AND PARMEGGIAN1, P.L.
Mechanisms underlying hypothalamic temperature
changes during sleep in mammals. Brain Res.,
632: 136-142, 1993.
-
- 5. BAKER, M.A. AND HAYWARD, J.N. Carotid
rete and brain temperature of cats. Nature, 216:
139-141, 1967.
-
- 6. BAKER, MA. AND HAYWARD, J.N. Autonomic
basis for the rise in brain temperature during
paradoxical sleep. Science, 157: 1586-1588,
1967.
-
- 7. BUSIJA, D.W. AND HEISTAD, D.D. Factors
involved in the physiological regulation of the
cerebral circulation. Rev. Physiol. Biochem.
Pharmacol., 101: 162-211, 1984.
-
- 8. CABANAC, M. Keeping a cool head. News
Physiol. Sci., 1: 41-44, 1986.
-
- 9. CABANAC, M. Human Selective Brain
Cooling. Springer-Verlag, Heidelberg, 1995.
-
- 10. CABANAC, M. AND CAPUTA, M. Natural
selective cooling of the human brain: evidence
of its occurrence and magnitude. J. Physiol.,
Lond., 286: 255-264, 1979.
-
- 11. CALASSO, M. AND PARMEGGIANI, EL.
Thermogenesis of interscapular brown adipose
tissue selectively influences pontine and
preoptic-hypothalamic temperatures during sleep
in the rat. Brain Res., 1015: 103-106,
2004.
-
- 12. CALASSO, M., ZANTEDESCHI, E. AND
PARMEGGIANI, P.L. Cold-defense function of brown
adipose tissue during sleep. Am. J. Physiol.,
265: R1060-R1064, 1993.
-
- 13. CAPUTA, M., KADZIELA, W. AND NAREBSKI,
J. Significance of cranial circulation for the
brain homeothermia in rabbits. II. The role of
the cranial venous lakes in the defence against
hyperthermia. Acta Neurobiol. Exp., 36: 625-638,
1976.
-
- 14. CIANCI, T., ZOCCOLI, G., LENZI, P. AND
FRANZINI, C. Loss of integrative control of
peripheral circulation during desynchronized
sleep. Am. J. Physiol., 261: R373-R377,
1991.
-
- 15. DELGADO, J.M.R. AND HANAI, T.
Intracerebral temperatures in free-moving cats.
Am. J. Physiol., 211: 755-769, 1966.
-
- 16. DENOYER, M., SALLANON, M., BUDA, C.,
DELHOMME, G., DITTMAR, A. AND JOUVET, M. The
posterior hypothalamus is responsible for the
increase of brain temperature during paradoxical
sleep. Exp. Brain Res., 84: 326-334, 1992.
-
- 17. DUFOUR, R. AND COURT, L. Le débit
cérébral sanguin au cours du
sommeil paradoxal du lapin. Arch. Ital. Biol.,
115: 57-76, 1977.
-
- 18. EDVINSSON, L., MACKENZIE, ET. AND
MCCULLOCH, J. Cerebral Blood Flow and
Metabolism. Raven Press, New York, 1993.
-
- 19. FINDLAY, A.L.R. AND HAYWARD, J.N.
Spontaneous activity of single neurones in
hypothalamus of rabbits during sleep and waking.
J. Physiol., Lond., 201: 237-258, 1969.
-
- 20. FRANZINI, C. Brain metabolism and blood
flow during sleep. J. Sleep Res., 1:
3-16,1992.
-
- 21. FRANZINJ, C., CIANCI, T., LENZI, P. AND
GuIDAL0TrI, P.L. Neural control of vasomotion in
rabbit ear is impaired during desynchronized
sleep. Am. J. Physiol., 243: R142-R 146,
1982.
-
- 22. HALE, AR. Circle of Willis: functional
concepts, old and new. Am. Heart J., 60:
491-494, 1960.
-
- 23. HAYWARD, J.N. Brain temperature
regulation during sleep and arousal in the dog.
Exp. Neurol., 21: 201-212, 1968.
-
- 24. HAYWARD, J.N. AND BAKER, M.A. Role of
the cerebral arterial blood in the regulation of
brain temperature in the monkey. Am. J.
Physiol., 215: 389-403, 1968.
-
- 25. HAYWARD, J.N. AND BAKER, M.A. A
comparative study of the role of the cerebral
arterial blood in the regulation of brain
temperature in five mammals. Brain Res., 16:
417-440, 1969.
-
- 26. HELLER, H.C. Temperature,
Thermoregulation and Sleep. Pp. 292-304. In:
KRYGER, M.H., ROTH, T. AND DEMENT, W.C. (Eds.),
Principles and Practice of Sleep Medicine.
Philadelphia, Saunders, 2005.
-
- 27. HULL, CD., BUCHWALD, N.A., DUBROWSKY, B.
AND GARCIA, J. Brain temperature and arousal.
Exp. Neurol., 12: 238-246, 1965.
-
- 28. JESSEN, C. Temperature Regulation in
Humans and Other Mammals. Springer-Verlag,
Berlin, 2001.
-
- 29. JESSEN, C. AND KUHNEN, G. No evidence
for brain stem cooling during face fanning in
humans. J. Appl. Physiol., 72: 664-669,
1992.
-
- 30. KANZOW, E., KRAUSE, D. AND KUHNEL, H.
Die Vasomotorik der Hirnrinde in den Phasen
desynchronisierter EEG Aktivität im
naturlichen Schlaf der Katze. Pflugers Arch.
Gesamte Physiol., 274: 593-607, 1962.
-
- 31. KAWAMURA, H. AND SAWYER, C.H. Elevation
in brain temperature during paradoxical sleep.
Science, 150: 912-913, 1965.
-
- 32. KAWAMURA, H., WITHMOYER, D.I. AND
SAWYER, C.H. Temperature changes in the rabbit
brain during paradoxical sleep. EEG. Clin.
Neurophysiol., 21: 469-477, 1966.
-
- 33. KOVALZON, V.M. Brain temperature
variations during natural sleep and arousal in
white rats. Physiol. Behav., 10: 667-670,
1973.
-
- 34. MAQUET, P. Functional neuroimaging of
normal human sleep by positron emission
tomography. J. Sleep Res., 9: 207-231,
2000.
-
- 35. NIELSEN, B. AND JESSEN, C. Evidence
against brain stem cooling by face fanning in
severely hyperthermic humans. Pflugers Arch.,
422: 168-172, 1992.
-
- 36. PARMEGGIANI, P.L. Temperature regulation
during sleep: a study in homeostasis. Pp. 97-
143. In: OREM, J. AND BARNES, C.D. (Eds.),
Physiology in Sleep. Research Topics in
Physiology. New York, Academic Press, 1980.
-
- 37. PARMEGGIANI, P.L. The Autonomic Nervous
System in Sleep. Pp. 194-203. In: KRYGER, M.H.,
ROTH, T. AND DEMENT, W.C. (Eds.); Principles and
Practice of Sleep Medicine. Philadelphia,
Saunders, 1994.
-
- 38. PARMEGGIANI, P.L. Brain cooling across
wake-sleep behavioral states in homeothermic
species: an analysis of the underlying
physiological mechanisms. Rev. Neurosci., 6:
353363, 1995.
-
- 39. PARMEGGIANI, EL. Thermoregulation and
sleep. Frontiers in Bioscience, 8: s557-567,
2003.
-
- 40. PARMEGGIANI, P.L., AGNATI, L.F.,
ZAMBONI, G. AND CIANCI, T. Hypothalamic
temperature during the sleep cycle at different
ambient temperatures. EEG. Clin. Neurophysiol.,
38: 589-596, 1975.
-
- 41. PARMEGGIANI, EL., AZZARONI, A. AND
CALASSO, M. A pontine-hypothalamic temperature
difference correlated with cutaneous and
respiratory heat loss. Respir Physiol., 114:
4956, 1998.
-
- 42. PARMEGGIANI, P.L., AZZARONI, A. AND
CALASSO, M. Systemic hemodynamic changes raising
brain temperature in REM sleep. Brain Res., 940:
55-60, 2002.
-
- 43. PARMEGGIANI, P.L., CALASSO, M. AND
ZoccoLi G. Decrease in the carotid share of
cerebral blood flow during REM sleep. J. Sleep
Res., 11, (Suppl. 1): 169, 2002.
-
- 44. PARMEGGIANI, P.L., FRANZINI, C., LENZI,
P. AND CIANcI, T. Inguinal subcutaneous
temperature changes in cats sleeping at
different environmental temperatures. Brain
Res., 33: 397-404, 1971.
-
- 45. PARMEGGIANI, P.L., ZAMBONI, G., CIANcI,
T. AND CALASSO, M. Absence of thermoregulatory
vasomotor responses during fast wave sleep in
cats. EEG. Clin. Neurophysiol., 42:372-380,
1977.
-
- 46. PARMEGGIANI, P.L., ZAMBONI, G., PEREZ,
E. AND LENZI, P. Hypothalamic temperature during
desynchronized sleep. Exp. Brain Res., 54:
315-320, 1984.
-
- 47. REITE, M.L. AND PEGRAM, G.V. Cortical
temperature during paradoxical sleep in the
monkey. EEG. Clin. Neurophysiol., 25: 36-41,
1968.
-
- 48. REIVICH, M. Regional cerebral blood flow
in physiologic and pathophysiologic states. Pp.
191-228. In: MEYER, J.S. AND SCHADE, J.P.
(Eds.), Cerebral Blood Flow. Progr. Brain Res.
Amsterdam, Elsevier, 35: 1972.
-
- 49. RISBERG, J. AND INGVAR, D.H. Increase of
regional cerebral blood volume during REMsleep
in man. Pp. 384-388. In: KOELLA, W.P. AND LEVIN,
P. (Eds.), Sleep: proceedings of the first
european congress on sleep research. Basel,
Karger, 1973.
-
- 50. ROUSSEL, B., DITTMAR, A. AND CHOU VET,
G. Internal temperature variations during the
sleep wake cycle in the rat. Waking Sleeping, 4:
63-75, 1980.
-
- 51. SATOH, T. Brain temperature of the cat
during sleep. Arch. Ital. Biol., 106: 73-82,
1968.
-
- 52. SEROTA, H.M. Temperature changes in the
cortex and hypothalamus during sleep. J.
Neurophysiol., 2: 42-47, 1939.
-
- 53. SEROTA, H.M. AND GERARD, R.W. Localized
thermal changes in the cat's brain. J.
Neurophysiol., 1: 115-124, 1938.
-
- 54. SEYLAZ, J., MAM0, H., GOAS, J.Y.,
MAcLE0D, P., CARON, J.P. AND HOUDART, R. Local
cortical blood flow during paradoxical sleep in
man. Arch. Ital Biol., 109: l-14, 1971.
-
- 55. SHAPIRO, C.M. AND ROSENDORFF, C. Local
hypothalamic blood flow during sleep. EEG. Clin.
Neurophysiol., 39: 365-369, 1975.
-
- 56. TACHIBANA, S. Relation between
hypothalamic heat production and intra- and
extracranial circulatory factors. Brain Res.,
16: 405-416, 1969.
-
- 57. VAN TWYVER, H. AND ALLISON, T. Sleep in
the opossum Didelphis marsupialis. EEG. Clin.
Neurophysiol., 29: 181-189, 1970.
-
- 58. VAN TWYVER, H. AND ALLISON, T. Sleep in
the armadillo Dasypus novemcinctus at moderate
and low ambient temperatures. Brain Behav.
Evol., 9: 107-120, 1974.
-
- 59. WALKER, J.M., WALKER, L.E., HARRIS, DV.
AND BERGER, R.J. Cessation of thermoregulation
during REM sleep in the pocket mouse. Am. J.
Physiol., 244: R114-R1 18, 1983.
-
- 60. WURTZ, R.H. Physiological correlates of
steady potential shifts during sleep and
wakefulness. II. Brain temperature, blood
pressure, and potential changes across ependyma.
EEG. Clin. Neurophysiol., 22: 43-53, 1967.
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