Changes in the sleep-wakefulness rhythm after chronic bilateral interruption of the middle cerebellar peduncles in the cat

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Changes in the sleep-wakefulness rhythm after chronic bilateral interruption of the middle cerebellar peduncles in the cat

Previous acute and chronic experimentsl-a, 5 led us to conclude that the cerebellum, through its fastigial 'ascending' output, exerts a tonic influence on diffuse electrocortical activity. This action is dual in sign, both desynchronizing and synchronizing. The latter, however, is the prevailing effect in freely moving cats, as is proved by the EEG effects of fastigial stimulation or inactivation, and also by the shift toward wakefulness that is regularly observed in the sleep wakefulness rhythm after bilateral fastigial lesions. As a further step in our investigation it seemed of interest to ascertain the role played by the cerebellar input in modifying the tonic 'ascending' influence exerted through the fastigial output. The present experiments were planned to identify the action exerted in this connection by the ponto-cerebellar afferents, namely by the main cerebellopetal pathway from the brain stem. We began our study by ascertaining whether chronic bilateral interruption of the middle cerebellar peduncles (brachia pontis) induced some changes in the sleep-wakefulness rhythm. Nine freely moving, chronically implanted adult cats, carefully conditioned to live in a sound-attenuated, roughly thermostatic recording cage, were used for daily experimental sessions lasting 12 h (from 9 a.m. to 9 p.m.). Electroencephalographic, electromyographic (neck muscles) and electrooculographic records were taken continuously, and behavioural correlates were observed, in each session, total durations of wakefulnesss, synchronized sleep and desynchronized sleep were measured, as were episode numbers and mean duration of episodes. The prerequisite for obtaining workable data was the definition of reliable average values in each intact preparation. To obtain such values, at least 10 pre-operative sessions were held. Their number was adequately increased (up to 33 in a single preparation) when the scattering of the daily values was such as to require a longer time basis. Two out of the 9 cats implanted had to be discarded because of excessive variability of their daily values. For the second stage of the experiments, 5 cats were submitted to bilateral peduncular lesions and two were used as controls. One of these underwent bilateral lesions in the cerebellar cortex overlying the middle cerebellar peduncle, and the other was submitted to a unilateral partial lesion of the middle cerebellar peduncle. All lesions were performed electrolytically, by means of electrodes acutely inserted, when needed, through steel tubing which had been stereotaxically implanted at the time of the aseptic preliminary surgery. In this way, no surgical procedure or narcosis was required for the actual production of the lesions, and a gap in the recording sessions was avoided. When the observations had continued for a sufficient time after the cerebellar lesions (16-35 days), the animals were killed, and histological controls of the lesion placements were performed on frozen serial sections (Nissl staining). All data were quantified. Means and standard errors were calculated, and all relevant differences were checked for their statistical significance (t test). For each animal and for both the pre- and post-lesion periods, the 'total sleep/wakefulness ratio' (TS/W) Brain Research, 26 (1971) 195-199

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Fig. 1. Modifications of the sleep-wakefulness rhythm, as observed in a typical experiment of bilateral interruption of middle cerebellar peduncles (cat BP t). The 3 histograms show, respectively, the total time ( i S.E., dotted area) spent in wakefulness (W), synchronized sleep (SS) and desynchronized sleep (DS), for each daily session. The arrows mark the time at which the bilateral peduncular lesion was performed. Note definite reduction of duration °fwakefulness a n d t h e c°rresp°nding increase of synchronized sleep.

Brain Research. 26 (1971) 195-199

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BP 1 rostral

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Fig. 2. Histological lesions (sketched from microphotographs) performed in the cat BP l submitted to bilateral coagulation of the middle cerebellar peduncles. Guiding tubing placements are indicated by dashed contours. SCP, MCP and ICP, superior, middle and inferior cerebellar peduncles; F, I, D, fastigial, interposital and dentate nuclei. was also calculated. The experimental observations lasted for a total of 3,288 h distributed over 274 recording sessions. Although obtained from non-circadian sessions, the results show that chronic interruption of the middle cerebellar peduncles does modify the sleep-wakefulness rhythm in the cat. Actually, changes were consistently observed in all animals submitted to this interruption and were not present in the control animals. They were not related to the motor disturbances following the peduncular lesions (hypokinesia, hypotonia and dysmetria), since the modifications of the sleep-wakefulness rhythm were stable, whereas in the present experiments the motor disturbances showed a clear-cut tendency to an early recovery. Actually, the first signs of regression of these disturbances appeared during the second or third day after the interruption, and the spontaneous motor behaviour of our animals was practically back to normal within Brain Research, 26 (1971) 195-199

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TABLE I MEAN TOTAL DURATIONS OF WAKEFULNESS, SYNCtlRONIZED SLEEP AND DESYNCHRONIZED SLEEP, AS MEASURED IN A TYPICAL EXPERIMENT (CAT B P 1 ) BEFORE AND AFTER BILATERAL LESIONS OF THE MIDDLF CEREBELLAR PEDUNCLES

Session

(a) 1-11(pre-lesion) (b) 12-37(post-lesion) t test for differences * P

-

Mean total duration per session (rain ~ S.E.) Wakefulness

Synchr. sleep

Desynchr. sleep

114.63 t_. 6.53 55.11 ~ 4.25 7.583*

515.81 :~ 6.08 581.96 £ 6.86 5.762*

89,54 5~68 82.92 : 4,98 0,766

0.001.

TABLE 1t TOTAL SLEEP WAKEFULNESS RATIOS I'WZ/W) AS CALCULATED FOR THE PRE- AND POST-OPERATIVE PERIODS IN CHRONIC PREPARATIONS SUBMITTED TG MIDDLE PEDUNCULAR LESIONS AND TO CONTROl.. LESIONS

BP 1-BP 5, peduncular lesions: C I-C 2. control lesions. Numbers in parentheses refer to thenumber of pre- and post-operative sessions. Preparation

BP 1 BP 2 BP 3 BP4 BP 5 CI C2

Observation periods Pre-operative

Post-operative

5.27(11 ) 3.18 (23) 3.83 (14} 3.22(111 2.90~ 33) 3.53 (181 6.35(111

12.20(261 6.44~241 7.06 (35t 7.89(171 4.47 ( 17/ 2.98q 191 5.87q 161

a week. The changes o f the sleep-wakefulness rhythm are exemplified in Fig. 1 and Table I, and the related peduncular lesions can be appreciated in Fig, 2. which refers to the same cat. The effects became a p p a r e n t during the same session in which the peduncular coagulations were performed. Essentially, the effects consisted o f a definite reduction o f the duration o f wakefulness and in a corresponding increase o f synchronized sleep, episodes o f which grew significantly longer. These changes are reflected in marked increases o f T S / W ratios (Table IlL As to desynchronized sleep, the mean values showed no significant differences as c o m p a r e d with those obtained in the pre-lesion period. These variations persisted until the end o f the observation period (16-35 post-operative sessions) and the quantitative differences proved to be statistically significant (Table I). The present results support the hypothesis that ponto-cerebellar afferents might be involved in the normal regulation o f the vigilance level. In view o f the previous results 3 on the effects o f fastigial coagulation, such an involvement might be accounted for by the projections sent t h r o u g h the middle cerebellar peduncles to the vermian Brain Research. 26 (1971) 195-199

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cortex 4, since it has already been shown that interposital and dentate lesions are totally ineffective on the electrocortical tone 2,3. Ponto-cerebellar projections should exert an inhibitory effect on the functional level of the fastigial nuclei, whose synchronizing action has already been shown. Thus, the present results might be regarded as due to a release effect. This investigation was supported in part by a grant from the Consiglio Nazionale delle Ricerche. Institute of Human Physiology, University of Catania, Catania (Italy)

ROCCO RAFFAELE SALVATORE SAPIENZA ANTONIO URBANO MARGHERITA VENTURA

1 FADIGA,E., MANZONI,T., SAPIENZA,S., AND URBANO,A., Synchronizing and desynchronizing fastigial influences on the electrocortical activity of the cat, in acute experiments, Electroenceph. olin. Neurophysiol., 24 (1968) 330-342. 2 FADIGA,E., MANZONI,T., AND URBANO,A., The tonic action of fastigial efferents on the electrocortical activity, as appearing from acute ablation experiments in the cat, Arch. Sci. biol. (Bologna), 51 (1967) 24-40. 3 GIANNAZZO,E., MANZONI,T., RAFFAELE,R., SAP1ENZA, S., AND URBANO, A., Effects of chronic fastigial lesions on the sleep-wakefulness rhythm in the cat, Arch. ital. Biol., 107 (1969) 1-18. 4 JANSEN,J., ANt) BRODAL,A., Aspects of Cerebellar Anatomy, Grundt Tanum, Oslo, 1954, p. 121. 5 MANZONI,T., SAneNZA,S., AND URaAr~O,A., EEG and behavioural sleep-like effects induced by the fastigial nucleus in unrestrained, unanaesthetized cats, Arch. ital. Biol., 106 (1968) 61-72. (Accepted November 24th, 1970)

Brain Research, 26 (1971) 195-199