Sleep in the dove Zenaida asiatica

BEHAVIORAL AND NEURAL BIOLOGY

49, 133-138 (1988)

Sleep in the Dove Zenaida asiatica FRUCTUOSO AYALA-GUERRERO t AND IRENE VASCONCELOS-DUENAS

Departamento de Fisiologia, Instituto de Investigaciones Biomddicas, UNAM, Ciudad Universitaria, 04510 Mdxico, D.F. Electrographic and behavioral observations were made in five adult birds of the genus Zenaida asiatica. Five different vigilance states were quantitated: (1) Active waking (Aw) was characterized by constant behavioral activity; the nuchal electromyogram was tonically active with bursts associated to movements. The electroencephalographic pattern was low voltage and high frequency. (2) Quiet waking (Qw) was characterized by diminished behavioral activity and the EEG pattern was similar to that of Aw. (3) Drowsiness (D) was characterized by behavioral calm. Frequency of cerebral activity diminished progressively, but there were short periods of desynchronization corresponding to brief awakenings. (4) Slow wave sleep (SWS); during this period there was behavioral rest and EEG pattern of continuous slow waves and the nuchal EMG was tonically reduced. Spindles of sleep were not observed. (5) Paradoxical sleep (SP), behaviorally characterized by phasic manifestations consisting of noddings originated by rapid falling down of head and bursts of rapid eye movements. EEG activity was like that of waking state. EMG activity was maintained at the same level as during SWS but sometimes it decreased lightly. Total atonie was not observed. Sleep percentages were higher when recordings were done during the nocturnal period. © 1988 Academic Press, lnc

Slow wave and paradoxical sleep have been described in mammals and scrupulously analyzed in some of them such as the cat, the rat and others. These sleep phases have also been reported in birds. Behavioral characteristics of sleep in birds coincide with particular electrophysiological signs. A high percentage of the sleeping period is occupied by slow wave sleep, which is characterized by very low motor activity and by an electroencephalographic pattern of high voltage slow waves. Moreover, the nuchal electromyogram intensity is lower than that observed during wakefulness. The eye movements in the course of this phase of sleep become scarce and usually disappear, shortly before paradoxical sleep is installed. The electrophysiological signs of paradoxical sleep in birds are constituted by an EEG activity of fast frequency and low voltage that resembles the one described for the waking state. Furthermore, To whom reprint requests should be addressed. 133 0163-1047/88 $3.00 Copyright © 1988 by Academic Press, Inc. All rights of reproduction m any form reserved.

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AYALA-GUERRERO AND VASCONCELOS-DUEiqAS

there are bursts of rapid eye movements, except in some birds like the owls Speotyto cunicularia hypugaea (Berger & Walker, 1972) and Strix aluco (Susi6 & Kovacevfc, 1973), where the eyes are imprisoned inside the orbital bones. During this phase, an additional decrease of muscular activity is also observed, but it does not generally reach total atonie. On the other hand, a drowsiness phase has been considered (Van Twyver & Allison, 1972; Susi6 & Kovacevic, 1973), although its consistence is still electrophysiologically unclear. Studies on birds' sleep have been mainly carried out in chickens (Klein, Michel, & Jouvet, 1964; Peters, Vonderahe, & Schmid, 1965; Hishikawa, Cramer, and Kuhlo, 1969), domestic species like the pigeon (Tradardi, 1966; Van Twyver and Allison, 1972; Walker & Berger, 1972), and some wild birds such as the Falconiformes Buteo jamaicensis aborealis and Herpetotheres cachinnans chapmanni (Rojas-Ramirez & Tauber, 1970), the owl Strix aluco (Susi6 & Kovacevic, 1973), the giant petrel Macroneptes giganteus (Tomo, Panizza, & Castello, 1973) and the dove Streptopelia risoria (Walker, Walker, Palca, & Berger, 1983) among others. To our knowledge there are a few reports concerning the sleep of birds. Therefore, the present study was undertaken to characterize both the behavioral and electrophysiological sleep patterns in this bird not previously studied. Five adult specimens of the bird Zenaida asiatica, of both sexes, were used as experimental subjects. Under nembutal anesthesia (35 mg/kg, ip), feathers of both dorsolateral cephalic and nuchal regions were removed and the skull was left exposed by means of a longitudinal incision in the middle head. Cerebral activity was recorded with pairs of stainless steel electrodes placed on the surface of the right and left dorsolateral cortical regions. Eye movements were detected with two stainless steel screws implanted above the orbital edge. Wire loops inserted inside the superficial nuchal muscle recorded muscular activity. All electrode leads were soldered to a plug, which was firmly fixed to the skull with acrylic dental cement. After surgery, the doves were maintained in individual cages. Food and water were continuously available. Recordings were begun at least 30 days after postoperative recovery. A week prior to each recording the bird cage was placed in a sound-deadened environmental chamber under a 12-h light/12-h dark cycle (lights on at 07:00 h). In addition, a dim red light was kept continuously illuminated making behavioral monitoring possible during the dark period. The chamber was kept at a temperature of 23 ___ 3°C. Polygraphic recordings were made on a Grass Model III D electroencephalograph during 24 consecutive hours. Paper speed was 3 mm/s. During this period the animals were frequently observed in order to correlate their behavior with the polygraphic data. Thus we could obtain behavioral correlates of vigilance states exhibited by subjects. Five vigilance states were distinguished in Zenaida asiatica: active

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waking (Aw), quiet waking (Qw), drowsiness (D), slow wave sleep (SWS), and paradoxical sleep (PS). During Aw (Fig. 1A), the birds exhibited continuous head and body movements. Eye movements were also frequently observed. The electrical activity of the brain was characterized by waves of low voltage (less than 50/iV) and high frequency (more than 5 Hz), excepting the artifacts of high voltage and low frequency caused by the animal movements. In this state of vigilance neck EMG was tonically active with frequent phasic bursts associated with movements. When the animals were in Qw period, the general motor activity was diminished but eye movements and blinking still occurred frequently. The EEG was essentially unchanged compared with that of Aw, although occasional slow activity was seen, especially before the onset of drowsiness. The transition from Qw to D and from D to SWS was gradually achieved. The D state was behaviorally distinguished, because the bird looked for a comfortable position on its perch and assumed the sleeping position; after a certain time eye movements started to be less frequent. During this period, the frequency of cerebral activity was progressively reduced, but short periods of desynchronization corresponding to brief awakenings were also observed (Fig. 1B). The passage from D to SWS was progressive and the delimitation between

136

AYALA-GUERRERO AND VASCONCELOS-DUElqAS

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these two vigilance states was somewhat arbitrary, but the established criterion was that a definite and continuous slow wave activity was present in brain recordings to be considered as SWS (Fig. 1C). In this state the EEG revealed increased slow waves (2-4 Hz and 150 /zV) without spindles. Slow waves usually appeared in short epochs, lasting from several seconds up to 3 min. SWS was frequently interrupted by short behavioral and electrographical awakenings. Blinking was replaced by periods of complete palpebral closure and eyes remained closed. Eye movements persisted only with reduced frequency and amplitude. The tonic level of EMG activity decreased at the onset of SWS and there was a total absence of phasic burst activity seen during wakefulness and PS. During the course of SWS, cerebral activity was periodically desynchronized and the sleep posture was interrupted by phasic manifestations of rapid eye movements and noddings originated by rapid falling down of head, as if there was a sudden loss of muscle tone in the nape. The maximum muscular relaxation of neck was usually not reached at once but step by step, with a series of successive drops and head arrests. These episodes corresponding to PS were always preceded by SWS, occurring repeatedly and irregularly with individual periods lasting a few seconds with a mean of 7.6 -_- 5 s. The EEG patterns of PS were characterized by fast low voltages waves (less than 50/~V), which could not be differentiated from those in the awake alert state (Fig. 2). The percentage of total record time spent by the animals in each vigilance state was taken in relation to illumination conditions (Table 1). When studies were carried out under constant light conditions, an elevated value was obtained for wakefulness as compared to darkness recordings TABLE 1 07:00-19:00 h Light Period W D SWS PS

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SLEEP IN THE DOVE Zenaida asiatica

137

(p < .05). Sleep values were significantly high in darkness since both SWS (p < .01) and PS (p < .001) increased noticeably. The increase of PS during the dark period occurs in the frequency but not in the duration of PS phase. The polygraphic manifestations of wakefulness and sleep in Zenaida asiatica are similar to those findings previously reported in other birds (Berger & Walker, 1972; Van Twyver & Allison, 1972; Susid & Kovacevfc, 1973; Walker & Berger, 1972), placental mammals (Sterman, Knauss, Lehmann, & Clemente, 1965; Van Twyver, 1969; Adams & Barrat, 1974), and marsupials (Van Twyver & Allison, 1970; Astic & Royet, 1974). The present data indicate that the sleep phase characterized by head falling, neck muscle hypotonie associated with ocular movements and a cerebral activity of low voltages fast waves, is comparable to paradoxical sleep of other birds and mammals studied up to data. However, there are some aspects that must be compared. Unlike mammals, the neck muscle tone is not totally abolished, moreover, the episodes of PS are of very short duration. It seems likely that the nonabolition of muscular tone and the short duration of this sleep stage might be an adaptive mechanism to prevent the birds from falling. It has been suggested that paradoxical sleep in birds is interrupted by phasic labyrinthine reflexes which are elicited by the dropping of the head (Tradardi, 1966). However, this hypothesis is refuted by Walker and Berger's results (1972) on pigeons which, restrained in a sling in a stereotaxic instrument which rendered their heads stably supported, still presented brief episodes of PS. Similarly, these short periods were observed in domestic geese associated with muscular atonie (Dewasmes, Cohen-Adad, Koubi, & Le Maho, 1985) whenever they slept with their heads supported on their back. On the other hand, the present study shows that SWS was not differentiated into two stages such as exists in some mammals (Ursin, 1968). In this case, the high amplitude slow waves phase was occurring in absence of the spindle stage. In other birds, the undifferentiation of two SWS stages has also been pointed out (Ookawa & Gotoh, 1965; Tradardi, 1966; Ookawa, 1967; Hishikawa, Cramer, & Kuhlo, 1969; Walker & Berger, 1972). In mammals the elaboration of spindles during sleep depends on the integrity of the neocortex (Jouvet, 1962) and birds do not have a well unfolded neocortex, then it is possible that the SWS differences between birds and mammals may be explained in terms of degree of brain development. REFERENCES Adams, P. M., & Barrat, E, S. (1974). Nocturnal sleep in squirrel monkeys. Electroencephalography and Clinical Neurophysiology, 36, 201-204. Arirns-Kappers, C. U., Huber, G. C., & Crosby, E. C. (1936). The comparative anatomy of the nervous system of vertebrate, including man. New York: Macmillan Astic, L., & Royet, J. P. (1974). Sommeil chez le rat-kangourou, Potorous apicalis Etude

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