Brain Temperature Variations with Paradoxical Sleep: Implications for Relationships among EEG, Cerebral Metabolism, Sleep, and Consciousness

Allan Rechtschaffen, Paul Cornwell, William Zimmerman, and Marvin Bassan

University of Chicago


Proceedings of the Lyon Symposium on Sleep and Consciousness, December 1965.


This study was supported by Grant M-04151 and by Research Career Program Award MH-K3-18,428 from the National Institute of Mental Health, U.S. Public Health Service to Allan Rechtschaffen.

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Abstract

Increased unit firing rates in several brain areas (Bizzi et al. 1964; Evarts 1962, 1964; Huttenlocher 1961) and the dreams of humans (Aserinsky and Kleitman 1953; Dement and Kleitman 1957) during paradoxical sleep suggest increased cerebral metabolism during these periods. This possibility was studied by using variations in brain temperature in the cat as an index of changes in cerebral metabolism. Preliminary reports of increased brain temperature during paradoxical sleep have come recently from three different laboratories (Hanai and Delgado 1965; Kawamura and Sawyer 1965; Rechtschaffen et al. 1965). This report will document further and elaborate upon brain temperature-paradoxical sleep relationships and will consider their implications for the correlation between sleep, consciousness, EEG, and cerebral metabolism.

Method

Thermistors (Yellow Springs #44005) were chronically implanted in several brain sites of 12 cats, along with electrodes for recording EEG, eye movements (EOG), and nuchal muscle tone (EMG). The thermistors were rated as accurate to within 0.2°C, and our own tests showed that randomly selected pairs of thermistors were matched with each other well within these limits. The thermistors were insulated with vinyl and had time constants of about 2 sec. Recordings were made on a Beckman Type R Dynograph, using the 9858 thermistor coupler for temperature recordings. Calibration for absolute temperature was made with 0.01% accurate resistors and resistance equivalent values provided by the thermistor manufacturer. Recordings were made from unanesthetized and unrestrained cats in sound insulated cages and relatively stable temperature environments.

Results

Brain Temperature and Paradoxical Sleep

From 13 to 70 PSPs (paradoxical sleep periods) were recorded from each cat, producing a total of 437 PSPs. In eight cats, temperature was recorded from more than one brain site, producing a total of 689 separate temperature recordings during PSPs. The only restrictions in selection of data were that the recording be technically good and that the PSP be at least 2 min. long. Because brain temperature frequently continued to increase throughout the first 2 min. of a PSP or longer, the selection of short PSPs would produce unrepresentative values for the magnitude of the temperature rises.

Brain temperature increased at the start of all but 19 of the 689 PSP recordings. Most of the 19 PSP temperature declines came from one thermistor in one cat. Table I summarizes the data on magnitude of PSP brain temperature rise. Typically, the maximal rise during a PSP was between 0.1°C and 0.4°C, although individual rises were as large as 0.7°C.

The values for cortical temperature rise recorded from epidural thermistors were probably masked by temperature gradients across the dura; subcortical values were considerably higher than cortical values in two cats with epidural cortical thermistors, but approximated cortical values in cats with subdural cortical thermistors.

Table I. Brain Temperature Increases during Paradoxical Sleep
CatNo. of PSPsThermistor LocationMean max. rise °CS.D.No. of drops*Anat. Verif.†
Michel69Longitudinal fissure.18.101+
Bill20Third ventricle.18.101+
Francois69Cortex – epidural.16.081+
Danielle24Cortex – epidural.17.090+
Ian70Cortex – epidural.13.070+
Parahippocampal gyrus.22.090+
Donald55Cortex – epidural.10.040+
Anterior commisure.18.070+
Sigmund20Cortex – frontal epidural.16.063+
Cortex – occipital epidural.09.0713+
Willy20Cortex – frontal epidural.44.150+
Cortex – occipital epidural.30.100+
Cay20Cortex – occipital subdural.28.090+
Preoptic nucleus.30.130o
Paul21Cortex – occipital subdural.16.060+
Hippocampus – ventral.16.070o
Betty13Cortex – occipital epidural.14.040+
Cortex – occipital subdural.18.060+
Pons.10.030o
Louise20Preoptic nucleus – rostral.29.060o
Preoptic nucleus – caudal.26.050o
Lateral geniculate nucleus.28.080o
* Indicates the number of paradoxical sleep periods during which a drop in temperature was recorded. These periods are not included in the calculation of mean maximal rise (difference between temperature at the start of a paradoxical sleep period and the maximal temperature for that period).
† Continuing experimentation with these cats precludes verification of anatomical site for those stereotaxically implanted thermistors indicated with an "o".

While all brain sites studied showed PSP temperature rises, little can be said about regional differences in rise magnitude from the small number of unsystematically selected recording sites. Furthermore, unless temperature gradients are evaluated, it is difficult to know whether changes recorded at a specific site represent physiological changes at that site or heat transfer from other areas. Differences among cats in brain temperature rise during PSPs were more striking than regional differences in the same cat.

Figures 1, 2, and 3 show the typical course of variations in brain temperature during PSPs: a relatively stable brain temperature level during slow wave sleep (high voltage EEG, presence of tonic EMG, and virtual absence of rapid eye movements) and a fairly abrupt rise with the start of paradoxical sleep (low voltage EEG, absence of tonic EMG, and the presence of rapid eye movements). The specificity of the temperature rise to PSP is seen most clearly in Fig. 2 where there is a steep rise at the start of an "aborted" PSP, a steep decline during a short return to slow wave sleep, a rise and sustained elevation during a long PSP, and a steep decline with the final return to slow wave sleep. All three recordings represent the typical overall parallelism of temperature recordings from different brain sites.

Figure 1. Subcortical (parahippocampal gyrus), cortical (epidural), and intraperitoneal temperature changes in the transition from slow wave sleep to paradoxical sleep and from paradoxical sleep to wakefulness.
Figure 2. Brain temperature changes in the transitions between slow wave and paradoxical sleep.
Figure 3. Brain and intraperitoneal temperature changes in transitions between slow wave sleep, paradoxical sleep, and wakefulness.

A consistent sequence of changes in brain temperature, EEG, and EMG at the start of each PSP could have implications for possible PSP triggering mechanisms. At the very least, knowledge of such sequences would eliminate some of the possible causal relations among these variables. Initiation of each change is difficult to define with precision. Brain temperature shows continuous minute variation; EEG desynchronization is not abrupt; loss of tonic EMG, especially when viewed in integrated recordings, is almost always gradual. Therefore, the sequence of changes was defined by conservative criteria. "Preceding" was defined as a measure showing an unambiguous change (increase in temperature, decrease in EEG amplitude, loss of tonic EMG) from a prior stable baseline at least 30 sec. before a similarly unambiguous change in another physiological variable. If two measures changed within the same 30 sec. period, the changes were arbitrarily defined as having occurred at the same time. Using these criteria, temperature rises preceded EMG changes in 0.1% of PSPs and followed EMG changes in 23.5% of PSPs. Temperature rises preceded EEG changes in 18.9% of PSPs and followed EEG changes in 26.0% of PSPs. Thus, sometimes the temperature changes shortly preceded EEG and EMG changes at the start of PSPs, and sometimes shortly followed them, but most often the three changes occurred at about the same time.

In short PSPs the brain temperature usually described a smooth ascending curve, e.g., Fig. 1. In longer PSPs, brain temperature usually stabilized at a plateau on which there were minor variations, e.g., Fig. 2. Phasic dips in brain temperature during PSPs almost never reached pre-PSP baseline values. Momentary reappearance of tonic EMG or EEG slow waves during a PSP were always accompanied by corresponding dips in the brain temperature.

Typical changes at the end of PSPs are represented in Figs. 1, 2, and 3. With a return to slow wave sleep, brain temperature always declined, usually to about pre-PSP baseline level, e.g., Fig. 2. The temperature decline sometimes preceded, sometimes followed the EMG and EEG change by a short interval. If the cat awakened from a PSP, brain temperature could either decline, as in the short period of wakefulness at the end of the PSP in Fig. 1, remain at about the same level as in Fig. 3, or rise. When the cat was quiet or drowsy upon awakening, the waking brain temperature sometimes dropped from the PSP level; when the cat seemed alert or excited upon awakening, brain temperature was more likely to rise.

Basis of the Temperature Increase

Blood flow variations and/or metabolic heat production could conceivably cause the PSP brain temperature rises. Two factors should be evaluated to determine whether the brain temperature rises during PSPs are caused by blood flow variations: 1) the temperature of the brain with respect to the temperature of the blood entering the brain and 2) the amount of cerebral blood flow. For instance, if the temperature of the brain is higher than that of the blood entering it, an increase in cerebral blood flow should cool the brain, and a decrease in cerebral blood flow should result in a heating of the brain.

The finding of Feitelberg and Lampl (1935) that temperature in the carotid artery of awake, unanesthetized cats was consistently lower than the temperature of the cerebral cortex provides evidence that the temperature of the blood entering the brain is cooler than the brain. In humans, the temperature of the venous drainage of the brain is higher than intracardiac temperature, and the difference increases the closer to the brain the venous drainage is recorded (Eichna et al. 1951).