Seasonal influences on sleep and executive function in the migratory White-crowned Sparrow (Zonotrichia leucophrys gambelii).

BACKGROUND: We have previously shown that the White-crowned Sparrow (WCS) decreases sleep by 60% during a period of migratory restlessness relative to a non-migratory period when housed in a 12 h light: 12 h dark cycle. Despite this sleep reduction, accuracy of operant performance was not impaired, and in fact rates of responding were elevated during the migratory period, effects opposite to those routinely observed following enforced sleep deprivation. To determine whether the previously observed increases in operant responding were due to improved performance or to the effects of migration on activity level, here we assessed operant performance using a task in which optimal performance depends on the bird's ability to withhold a response for a fixed interval of time (differential-reinforcement-of-low-rate-behavior, or DRL); elevated response rates ultimately impair performance by decreasing access to food reward. To determine the influence of seasonal changes in day length on sleep and behavioral patterns, we recorded sleep and assessed operant performance across 4 distinct seasons (winter, spring, summer and fall) under a changing photoperiod. RESULTS: Sleep amount changed in response to photoperiod in winter and summer, with longest sleep duration in the winter. Sleep duration in the spring and fall migratory periods were similar to what we previously reported, and were comparable to sleep duration observed in summer. The most striking difference in sleep during the migratory periods compared to non-migratory periods was the change from discrete day-night temporal organization to an almost complete temporal fragmentation of sleep. The birds' ability to perform on the DRL task was significantly impaired during both migratory periods, but optimal performance was sustained during the two non-migratory periods. CONCLUSIONS: Birds showed dramatic changes in sleep duration across seasons, related to day length and migratory status. Migration was associated with changes in sleep amount and diurnal distribution pattern, whereas duration of sleep in the non-migratory periods was largely influenced by the light-dark cycle. Elevated response rates on the DRL task were observed during migration but not during the short sleep duration of summer, suggesting that the migratory periods may be associated with decreased inhibition/increased impulsivity. Although their daily sleep amounts and patterns may vary by season, birds are susceptible to sleep loss throughout the year, as evidenced by decreased responding rates following enforced sleep deprivation.

Sleep deprivation in pigeons and rats using motion detection.

STUDY OBJECTIVES: Forced sleep deprivation results in substantial behavioral and physiologic effects in mammals. The disk-over-water (DOW) method produces a syndrome characterized by increased energy expenditure and a robust preferentially rapid-eye-movement sleep rebound upon recovery or eventual death after several weeks of sleep deprivation. The DOW has been used successfully only in rats. This paper presents a method to enforce long-term controlled sleep deprivation across species and to compare its effects in rats and pigeons. DESIGN AND INTERVENTION: A conveyor was substituted for the DOW disk. Behavior rather than electroencephalography was used to trigger arousal stimuli, as in gentle-handling deprivation. Rats and pigeons were deprived using this apparatus, and the results were compared with each other and with published reports. MEASUREMENTS AND RESULTS: The physiologic consequences and recovery sleep in rats were like those published for DOW rats. Magnitude of sleep loss and recovery patterns in pigeons were similar to those seen in rats, but expected symptoms of the sleep deprivation syndrome were absent in pigeons. The use of a motion trigger allowed us to measure and, thus, to assess the quality and impact of the procedure. CONCLUSION: Prolonged and controlled sleep deprivation can be enforced using automated motion detection and a conveyor-over-water system. Pigeons and rats, deprived of sleep to the same extent, showed similar patterns of recovery sleep, but pigeons did not exhibit the hyperphagia, weight loss, and debilitation seen in rats.

Sleep deprivation in the pigeon using the Disk-Over-Water method.

A well-defined sleep deprivation (SD) syndrome has been observed in studies with rats under conditions of severe sleep loss on the Disk-Over-Water (DOW) apparatus. Observation of the sleep deprivation syndrome across taxa would assist in the elucidation of the function of sleep. In the present study, the effects of total sleep deprivation were assessed in pigeons, a biologically relevant choice given that birds are the only non-mammalian taxon known to exhibit unequivocal rapid-eye-movement (REM) sleep and non-REM (NREM) sleep. Pigeons were deprived of sleep for 24-29 days on the DOW by rotating the disk and requiring them to walk whenever sleep was initiated. Control (C) birds were also housed on the DOW and required to walk only when the deprived (D) birds were required to walk due to sleep initiation. NREM and REM sleep amounts were reduced from baseline during the deprivation for both D and C birds, although D birds obtained less NREM sleep than controls. Across the deprivation, D birds had their total sleep reduced by 54% of baseline (scored in 4 s epochs), whereas previous studies in rats on the DOW reported total sleep reduction of as much as 91% (scored in 30 s epochs). Pigeons proved to be more resistant to sleep deprivation by the DOW method and were much more difficult to deprive over the course of the experiment. Overall, the pigeons showed recovery sleep patterns similar to those seen in rats; i.e., rebound sleep during recovery was disproportionately composed of REM sleep. They did not, however, show the obvious external physical signs of the SD syndrome nor the large metabolic and thermoregulatory changes associated with the syndrome. The DOW method was thus effective in producing sleep loss in the pigeon, but was not as effective as it is in rats. The absence of the full SD syndrome is discussed in the context of limitations of the DOW apparatus and the possibility of species-specific adaptations that birds may possess to withstand or adapt to conditions of limited sleep opportunity.

Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii).

Twice a year, normally diurnal songbirds engage in long-distance nocturnal migrations between their wintering and breeding grounds. If and how songbirds sleep during these periods of increased activity has remained a mystery. We used a combination of electrophysiological recording and neurobehavioral testing to characterize seasonal changes in sleep and cognition in captive white-crowned sparrows (Zonotrichia leucophrys gambelii) across nonmigratory and migratory seasons. Compared to sparrows in a nonmigratory state, migratory sparrows spent approximately two-thirds less time sleeping. Despite reducing sleep during migration, accuracy and responding on a repeated-acquisition task remained at a high level in sparrows in a migratory state. This resistance to sleep loss during the prolonged migratory season is in direct contrast to the decline in accuracy and responding observed following as little as one night of experimenter-induced sleep restriction in the same birds during the nonmigratory season. Our results suggest that despite being adversely affected by sleep loss during the nonmigratory season, songbirds exhibit an unprecedented capacity to reduce sleep during migration for long periods of time without associated deficits in cognitive function. Understanding the mechanisms that mediate migratory sleeplessness may provide insights into the etiology of changes in sleep and behavior in seasonal mood disorders, as well as into the functions of sleep itself.

Acute effects of light and darkness on sleep in the pigeon (Columba livia).

In addition to entraining circadian rhythms, light has acute effects on sleep and wakefulness in mammals. To determine whether light and darkness have similar effects in birds, the only non-mammalian group that displays sleep patterns comparable to mammals, we examined the effects of lighting changes on sleep and wakefulness in the pigeon. We quantified sleep behavior (i.e., bilateral or unilateral eye closure) in pigeons maintained under a 12:12 LD cycle, and immediately following a change from a 12:12 to a 3:3 LD cycle. During both LD cycles, sleep was most prevalent during dark periods. During the 3:3 LD cycle, darkness had the greatest sleep promoting effect during the hours corresponding to the subjective night of the preceding 12:12 LD cycle, whereas light suppressed sleep across circadian phases. As previously suggested, the light-induced decrease in sleep in the subjective night might be partly mediated by the suppression of melatonin by light. Although the sleep promoting effect of darkness was modulated by the circadian rhythm, sleep in darkness occurred during all circadian phases, suggesting that darkness per se may play a direct role in inducing sleep. In addition to the effects of lighting on behavioral state, we observed an overall bias toward more right eye closure under all lighting conditions, possibly reflecting a response to the novel testing environment.

Sleep responses to light and dark are shaped by early experience.

Light regulates sleep timing through circadian entrapment and by eliciting acute changes in behavior. These behaviors are mediated by the subcortical visual system, retinorecipient nuclei distinct from the geniculocortical system. To test the hypothesis that early visual experience shapes light regulation of behavior, the authors recorded sleep in albino rats reared in continuous dark, continuous light, or a 12-hr light-dark cycle. Dark rearing strengthened and light rearing weakened acute responses to light, including light modulation of REM sleep, a marker for pretectal function in albino rats. However, neither dark nor light rearing altered daily amounts of wakefulness, non-REM sleep, or REM sleep. Thus, light and dark rearing might differentially affect the balance between acute and circadian responses to light that, in concert, govern sleep timing.