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

Ruth M Benca,William H Obermeyer,Martin Wikelski,Niels C Rattenborg,Bruce H Mandt,Reto Huber,Peter J Winsauer

doi:10.1371/journal.pbio.0020212

Ruth M Benca, William H Obermeyer + Show 5 more

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https://doi.org/10.1371/journal.pbio.0020212

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Abstract

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.

Highlights

Seasonal behaviors occur in virtually all organisms, ranging from insects to mammals (Goldman et al 2004)
The sleep patterns of birds in a migratory state were recorded in captivity, where migratory behavior manifests itself as migratory restlessness (Zugunruhe), i.e., nocturnal activity, including hopping and wing flapping (Berthold and Querner 1988; Berthold et al 2000)
An increase in drowsiness and a corresponding decrease in wakefulness were observed during the day, migrating sparrows did not compensate for sleep loss at night by sleeping more during the day or by increasing slow-wave sleep (SWS) intensity on migratory nights

Summary

Introduction

Seasonal behaviors occur in virtually all organisms, ranging from insects to mammals (Goldman et al 2004). Just as circadian rhythms allow organisms to anticipate daily cycles of light and dark, circannual behaviors such as migration allow them to predict and respond to seasonal changes in environmental conditions. Seasonal migratory behavior is both endogenously generated and shaped by external factors such as photoperiod length, weather, and food availability (Gwinner and Helm 2003). The most extraordinary examples of seasonal migration occur in birds, many species of which regularly migrate thousands of kilometers. One aspect of migration that is likely to impact all others, remains a complete mystery: Do birds sleep during migration and if so, how (Moore 1999; Schwilch et al 2002; Jenni and Schaub 2003)?

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