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Research Article

Characterization of Sleep in Zebrafish and Insomnia in Hypocretin Receptor Mutants

  • Tohei Yokogawa,

    Affiliation: Howard Hughes Medical Institute, Stanford University, Palo Alto, California, United States of America

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  • Wilfredo Marin,

    Affiliation: Howard Hughes Medical Institute, Stanford University, Palo Alto, California, United States of America

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  • Juliette Faraco,

    Affiliation: Stanford Center for Narcolepsy, Stanford University, Palo Alto, California, United States of America

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  • Guillaume Pézeron,

    Affiliations: Ecole Normale Supérieure, Paris, France, INSERM Unité 784, Paris, France

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  • Lior Appelbaum,

    Affiliation: Howard Hughes Medical Institute, Stanford University, Palo Alto, California, United States of America

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  • Jian Zhang,

    Affiliation: Stanford Center for Narcolepsy, Stanford University, Palo Alto, California, United States of America

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  • Frédéric Rosa,

    Affiliations: Ecole Normale Supérieure, Paris, France, INSERM Unité 784, Paris, France

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  • Philippe Mourrain,

    Affiliation: Stanford Center for Narcolepsy, Stanford University, Palo Alto, California, United States of America

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  • Emmanuel Mignot mail

    To whom correspondence should be addressed. E-mail: mignot@stanford.edu

    Affiliations: Howard Hughes Medical Institute, Stanford University, Palo Alto, California, United States of America, Stanford Center for Narcolepsy, Stanford University, Palo Alto, California, United States of America

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  • Published: October 16, 2007
  • DOI: 10.1371/journal.pbio.0050277

Reader Comments (2)

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Indeed, it does.

Posted by plosbiology on 07 May 2009 at 22:21 GMT

Author: Emmanuel Mignot
Position: Professor
Institution: Stanford University
E-mail: mignot@stanford.edu
Additional Authors: Jamie Zeitzer, Tohei Yokogawa, Philippe Mourrain
Submitted Date: November 30, 2007
Published Date: December 5, 2007
This comment was originally posted as a “Reader Response” on the publication date indicated above. All Reader Responses are now available as comments.

We thank Dr. Rial and colleagues for their comments. We, however, disagree with their interpretations of our work. Sleep in mammals can be defined using electroencephalography (EEG) and there are strong correlates of EEG patterns that can be observed in an animal’s behavior. Based on these correlates, a behavioral definition of sleep has been established that can be extended to animals with less well defined or no telencephalic tissue. By these criteria, sleep has been proposed to occur in fish, amphibians, reptiles, birds, and possibly insects [1,2]. While one could argue that all of the functions ascribed to mammalian sleep, especially those focused on neocortical activity, do not occur in sleep, it is likely that the functions of primitive sleep in non-mammalian vertebrates are recapitulated in vertebrate sleep.

Rial et al. contend that a circadian variation is necessary for sleep (“…control of circadian… during sleep, which should be recognized consequently as essential to define the presence of sleep…”). This is erroneous as mammals that have had an ablation of their circadian clock (SCN, suprachiasmatic nucleus) still exhibit sleep, albeit not organized by circadian time [3,4]. Barring this, however, there is abundant evidence that zebrafish display robust circadian control of locomotor rhythms. We clearly show this in supplementary figure S1, in which a cyclic pattern of activity is evident even though the fish are in constant light for 10 days and sleep was strongly suppressed by the light (not to mention that individual phases were not aligned in this graph). We also refer to the work of Dr. Greg M. Cahill that clearly demonstrates circadian organization of locomotion in the zebrafish [5].

Regarding homeostatic regulation, the observation of a sleep rebound after sleep deprivation by electrical stimulation only when animals are released in the dark is indeed puzzling. There is precedent in mammals and birds for the absence of or reduced homeostatic regulation of sleep in certain circumstances (e.g., migrating sparrows [6], neonatal cetaceans [7]). As noted by Dr. Rial, it could be argued that sleep rebound in our study is physical “fatigue”. While this is possible, we find this interpretation unlikely as our control fish were similarly electrically stimulated (and presumably as physically fatigued), and did not display a large rebound. Additionally, the fact rebound was not observed after the same conditions under light condition would argue against physical fatigue as this would not have been eliminated by light. Finally, other authors, most notably Dr. Irina Zhdanova, have also observed homeostatic sleep regulation in zebrafish using other techniques [8].

References
1. Campbell SS, Tobler I (1984) Animal sleep: a review of sleep duration across phylogeny. Neurosci Biobehav Rev 8: 269-300.
2. Shaw PJ, Cirelli C, Greenspan RJ, Tononi G (2000) Correlates of sleep and waking in Drosophila melanogaster. Science 287: 1834-1837.
3. Edgar DM, Dement WC, Fuller CA (1993) Effect of SCN lesions on sleep in squirrel monkeys: evidence for opponent processes in sleep-wake regulation. J Neurosci 13: 1065-1079.
4. Ibuka N, Kawamura H (1975) Loss of circadian rhythm in sleep-wakefulness cycle in the rat by suprachiasmatic nucleus lesions. Brain Res 96: 76-81.
5. Hurd MW, Debruyne J, Straume M, Cahill GM (1998) Circadian rhythms of locomotor activity in zebrafish. Physiol Behav 65: 465-472.
6. Rattenborg NC, Mandt BH, Obermeyer WH, Winsauer PJ, Huber R, et al. (2004) Migratory sleeplessness in the white-crowned sparrow (Zonotrichia leucophrys gambelii). PLoS Biol 2: E212.
7. Lyamin O, Pryaslova J, Lance V, Siegel J (2005) Animal behaviour: continuous activity in cetaceans after birth. Nature 435: 1177.
8. Zhdanova I (2006) Sleep in zebrafish. Zebrafish 3: 215-226.

No competing interests declared.