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Shivering and panting during sleep
SHORT COMMUNICATIONS
789
Shivering and panting during sleep It was previously reported that in unanaesthetized unrestrained cats a,a the phases of slow wave and fast wave sleep (the latter phase is also called activated ~ or paradoxical~ or deep~A 1 sleep) show a remarkable reduction in their mean total duration per experimental session when the environmental temperature markedly deviates from thermal neutrality (below 10°C and above 25°C). Spindle sleep, however, is scarcely affected in these conditions and only above 32-35°C its total duration per session decreases. This fact suggests that the changes in duration of slow wave and fast wave sleep cannot be simply a function of general arousal. In fact, they are more'likely t9 depend on specific changes in the activity of high integration levels in response to particular environmental temperatures. It was surmised that environmental temperature affects more markedly those phases of sleep which are characterized by processes that would compete with those underlying adaptive behaviour. Further to test this hypothesis the behaviour in sleep of specific thermal respanses such as shivering and panting was studied. The experiments were performed on unanaesthetized unrestrained cats carrying chronically implanted electrodes and transducers. Records (Grass electroencephalograph IIID and Grass polygraph 5D) were taken while the animals were in a thermoregulated box placed in a soundproof room. At low environmental temperatures (below 10°C: shivering threshold varies owing to individual and seasonal factors) shivering becomes particularly evident in the neck muscle E M G when the postural activity is reduced to a minimum, as occurs during spindle and slow wave sleep in curled up position. In this condition, bursts of spikes of great amplitude are superimposed on a more or less evident background of tonic postural activity (Fig. 1A). Rapid tremor of the skin of the neck is observed
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Fig. 1. Shivering during sleep at low environmental temperature (6°C). Cat 4, July. A: shivering is evident in the neck muscle EMG during slow wave sleep. B: shivering is absent during the subsequent phase of fast wave sleep. Hp, hippocampus dorsalis; P, parietal; EMG, electrogram of the neck muscles. by visual inspection. In the transition period from slow wave to fast wave sleep these bursts of spikes fade away together with the background tonus. Neck muscle activity of small amplitude may be detected only occasionally and at random during the phase of fast wave sleep (Fig. 1B). At high environmental temperatures (above 32°C: panting threshold varies Brain Research~
6 (1967) 789-791
790
SHORT COMMUNICATIONS
owing to individual and seasonal factors) panting (90-250/min) is present during both spindle and slow wave sleep (Fig. 2A). Panting disappears or undergoes a strong depression (30--80/rain) during the transition period from slow wave to fast wave sleep. This condition lasts t h r o u g h o u t the whole phase o f fast wave sleep (Fig. 2B).
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Fig. 2. Changes in respiratory rate during sleep at high environmental temperature (36.5°C). Cat 3, April. A: respiratory rate 246/rain during slow wave sleep. B: respiratory rate is reduced to 36/min during the subsequent phase of fast wave sleep. P, parietal; O, occipital; Hp, hippocampus dorsalis; EMG, electrogram of the neck muscles; RM, respiratory movements.
The absence of specific thermal responses in fast wave sleep of intact animals is remarkable as it may depend on a modification in hypothalamic integrative activity. Since the critical somatic and vegetative phenomena of fast wave sleep still occur in
decerebrate and pontine preparations1, 5 it is probable that, in intact animals, the changed hypothalamic o u t p u t during this phase o f sleep is responsible for the release o f brain stem structures from higher controls (steady stage of brain stem release). However, the basic changes in hypothalamic activity begin to develop before fast wave sleep, i.e. during late slow wave sleep (dynamic stage o f brain stem release), as shown by the onset o f progressing neck muscle h y p o t o n i a 1°, blood pressure alterations a,7, and modifications in respiratory rateS, o. O n this ground the specific modifications in duration o f both fast wave and slow wave sleep as a consequence o f deviations o f environmental temperature from thermal neutrality appear to be dependent on mechanisms designed to protect the actuation o f adequate adaptive behaviour.
Institute of Human Physiology, University of Bologna, Bologna (Italy)
PIER LUIGI PARMEGGIANI CLOTILDE RABINI
1 BARD, P., AND MAcrrr, M. B., The behaviour of chronically decerebrated cats. In G. E. W.
WOLST~NnOLI~ANDC. M. O'CONNOR(Eels.), NeurologicalBasis of Behaviour, Churchill, London, 1958, pp. 55-71. 2 DEr,irrzr, W. C., The occurrence of low voltage, fast, electroencephalogram patterns during behavioural sleep in the cat, Electroenceph. clin. Neurophysiol., 10 (1958) 291-296. 3 GuAzz/, M., AND ZANCHET'n,A., Blood pressure and heart rate during natural sleep of the cat and their regulation by carotid sinus and aortic reflexes, Arch. itaL Biol., 103 (1965) 789-817. 4 HUBEL,D. H., Electrocorticograms in cats during natural sleep, Arch. ital. Biol., 98 (1960) 171-181.
Brain Research, 6 (1967) 789-791
SHORT COMMUNICATIONS
791
5 JotrvET, M., Recherches sur les structures nerveuses et les m6canismes responsables des diff6rentes phases du sommeil physiologique, Arch. ital. BioL, 100 (1962) 125-206. 6 JOtrVET, M., MIC,EL, F., ET COURJON, J., Sur un stade d'activit6 61ectrique c6r6brale rapide au cours du sommeil physioiogique, C. R. Soc. Biol. (Paris), 153 (1959) 1024--1028. 7 KANZOW, E., KRAUSE, D., UNO KOh~EL, H., Die Vasomotorik der l-lirnrinde in den Phasen desynchronisierter EEG-Aktivit/it im natiirlichen Schlaf der Katze, Pfliigers Arch. ges. Physiol., 274 (1962) 593-607. 8 PARMEC,GIA~, P. L., E RAar~, C., Modificazioni deUe fasi del sonno nel gatto, per esposizione d i breve durata a d ifferenti temperature ambientali, Boll. Soc. itaL BioL sper., 43 (1967) 1079-1083. 9 PARMEGGIANI,P. L., AND RABINI, C., Sleep phases and environmental temperature, Heir. physioL Acta, 25 (1967) C R 214-CR 216. 10 PARMEGGIANI,P. L., AND ZANOCCO,G., A study on the bioelectrical rhythms of cortical and subcortical structures during activated sleep, Arch. ital. BioL, 101 (1963) 385--412. i I RossI, G. F., FAVALE,E., HARA, T., GIUSSA~, A., AND SACCO, G., Researches on the nervous mechanisms underlying deep sleep in the cat, Arch. itaL BioL, 99 (1961) 270-292. (Accepted October 16th, 1967)
Brain Research, 6 (1967) 789-791
789
Shivering and panting during sleep It was previously reported that in unanaesthetized unrestrained cats a,a the phases of slow wave and fast wave sleep (the latter phase is also called activated ~ or paradoxical~ or deep~A 1 sleep) show a remarkable reduction in their mean total duration per experimental session when the environmental temperature markedly deviates from thermal neutrality (below 10°C and above 25°C). Spindle sleep, however, is scarcely affected in these conditions and only above 32-35°C its total duration per session decreases. This fact suggests that the changes in duration of slow wave and fast wave sleep cannot be simply a function of general arousal. In fact, they are more'likely t9 depend on specific changes in the activity of high integration levels in response to particular environmental temperatures. It was surmised that environmental temperature affects more markedly those phases of sleep which are characterized by processes that would compete with those underlying adaptive behaviour. Further to test this hypothesis the behaviour in sleep of specific thermal respanses such as shivering and panting was studied. The experiments were performed on unanaesthetized unrestrained cats carrying chronically implanted electrodes and transducers. Records (Grass electroencephalograph IIID and Grass polygraph 5D) were taken while the animals were in a thermoregulated box placed in a soundproof room. At low environmental temperatures (below 10°C: shivering threshold varies owing to individual and seasonal factors) shivering becomes particularly evident in the neck muscle E M G when the postural activity is reduced to a minimum, as occurs during spindle and slow wave sleep in curled up position. In this condition, bursts of spikes of great amplitude are superimposed on a more or less evident background of tonic postural activity (Fig. 1A). Rapid tremor of the skin of the neck is observed
B
A I~
t
I
J
|J
Fig. 1. Shivering during sleep at low environmental temperature (6°C). Cat 4, July. A: shivering is evident in the neck muscle EMG during slow wave sleep. B: shivering is absent during the subsequent phase of fast wave sleep. Hp, hippocampus dorsalis; P, parietal; EMG, electrogram of the neck muscles. by visual inspection. In the transition period from slow wave to fast wave sleep these bursts of spikes fade away together with the background tonus. Neck muscle activity of small amplitude may be detected only occasionally and at random during the phase of fast wave sleep (Fig. 1B). At high environmental temperatures (above 32°C: panting threshold varies Brain Research~
6 (1967) 789-791
790
SHORT COMMUNICATIONS
owing to individual and seasonal factors) panting (90-250/min) is present during both spindle and slow wave sleep (Fig. 2A). Panting disappears or undergoes a strong depression (30--80/rain) during the transition period from slow wave to fast wave sleep. This condition lasts t h r o u g h o u t the whole phase o f fast wave sleep (Fig. 2B).
A ,
~1
'
i
J
~.
.
q
,
,
B
o
ill/'~
~
l; 2
2 sec
Fig. 2. Changes in respiratory rate during sleep at high environmental temperature (36.5°C). Cat 3, April. A: respiratory rate 246/rain during slow wave sleep. B: respiratory rate is reduced to 36/min during the subsequent phase of fast wave sleep. P, parietal; O, occipital; Hp, hippocampus dorsalis; EMG, electrogram of the neck muscles; RM, respiratory movements.
The absence of specific thermal responses in fast wave sleep of intact animals is remarkable as it may depend on a modification in hypothalamic integrative activity. Since the critical somatic and vegetative phenomena of fast wave sleep still occur in
decerebrate and pontine preparations1, 5 it is probable that, in intact animals, the changed hypothalamic o u t p u t during this phase o f sleep is responsible for the release o f brain stem structures from higher controls (steady stage of brain stem release). However, the basic changes in hypothalamic activity begin to develop before fast wave sleep, i.e. during late slow wave sleep (dynamic stage o f brain stem release), as shown by the onset o f progressing neck muscle h y p o t o n i a 1°, blood pressure alterations a,7, and modifications in respiratory rateS, o. O n this ground the specific modifications in duration o f both fast wave and slow wave sleep as a consequence o f deviations o f environmental temperature from thermal neutrality appear to be dependent on mechanisms designed to protect the actuation o f adequate adaptive behaviour.
Institute of Human Physiology, University of Bologna, Bologna (Italy)
PIER LUIGI PARMEGGIANI CLOTILDE RABINI
1 BARD, P., AND MAcrrr, M. B., The behaviour of chronically decerebrated cats. In G. E. W.
WOLST~NnOLI~ANDC. M. O'CONNOR(Eels.), NeurologicalBasis of Behaviour, Churchill, London, 1958, pp. 55-71. 2 DEr,irrzr, W. C., The occurrence of low voltage, fast, electroencephalogram patterns during behavioural sleep in the cat, Electroenceph. clin. Neurophysiol., 10 (1958) 291-296. 3 GuAzz/, M., AND ZANCHET'n,A., Blood pressure and heart rate during natural sleep of the cat and their regulation by carotid sinus and aortic reflexes, Arch. itaL Biol., 103 (1965) 789-817. 4 HUBEL,D. H., Electrocorticograms in cats during natural sleep, Arch. ital. Biol., 98 (1960) 171-181.
Brain Research, 6 (1967) 789-791
SHORT COMMUNICATIONS
791
5 JotrvET, M., Recherches sur les structures nerveuses et les m6canismes responsables des diff6rentes phases du sommeil physiologique, Arch. ital. BioL, 100 (1962) 125-206. 6 JOtrVET, M., MIC,EL, F., ET COURJON, J., Sur un stade d'activit6 61ectrique c6r6brale rapide au cours du sommeil physioiogique, C. R. Soc. Biol. (Paris), 153 (1959) 1024--1028. 7 KANZOW, E., KRAUSE, D., UNO KOh~EL, H., Die Vasomotorik der l-lirnrinde in den Phasen desynchronisierter EEG-Aktivit/it im natiirlichen Schlaf der Katze, Pfliigers Arch. ges. Physiol., 274 (1962) 593-607. 8 PARMEC,GIA~, P. L., E RAar~, C., Modificazioni deUe fasi del sonno nel gatto, per esposizione d i breve durata a d ifferenti temperature ambientali, Boll. Soc. itaL BioL sper., 43 (1967) 1079-1083. 9 PARMEGGIANI,P. L., AND RABINI, C., Sleep phases and environmental temperature, Heir. physioL Acta, 25 (1967) C R 214-CR 216. 10 PARMEGGIANI,P. L., AND ZANOCCO,G., A study on the bioelectrical rhythms of cortical and subcortical structures during activated sleep, Arch. ital. BioL, 101 (1963) 385--412. i I RossI, G. F., FAVALE,E., HARA, T., GIUSSA~, A., AND SACCO, G., Researches on the nervous mechanisms underlying deep sleep in the cat, Arch. itaL BioL, 99 (1961) 270-292. (Accepted October 16th, 1967)
Brain Research, 6 (1967) 789-791