Abstract
Early studies of the echidna led to the conclusion that this monotreme did not have rapid eye movement (REM) sleep. Because the monotremes had diverged from the placental and marsupial lines very early in mammalian evolution, this finding was used to support the hypothesis that REM sleep evolved after the start of the mammalian line. The current paper summarizes our recent work on sleep in the echidna and platypus and leads to a very different interpretation. By using neuronal recording from mesopontine regions in the echidna, we found that despite the presence of a high-voltage cortical electroencephalogram (EEG), brainstem units fire in irregular bursts intermediate in intensity between the regular non-REM sleep pattern and the highly irregular REM sleep pattern seen in placentals. Thus the echidna displays brainstem activation during sleep with high-voltage cortical EEG. This work encouraged us to do the first study of sleep, to our knowledge, in the platypus. In the platypus we saw sleep with vigorous rapid eye, bill and head twitching, identical in behaviour to that which defines REM sleep in placental mammals. Recording of the EEG in the platypus during natural sleep and waking states revealed that it had moderate and high-voltage cortical EEGs during this REM sleep state. The platypus not only has REM sleep, but it had more of it than any other animal. The lack of EEG voltage reduction during REM sleep in the platypus, and during the REM sleep-like state of the echidna, has some similarity to the sleep seen in neonatal sleep in placentals. The very high amounts of REM sleep seen in the platypus also fit with the increased REM sleep duration seen in altricial mammals. Our findings suggest that REM sleep originated earlier in mammalian evolution than had previously been thought and is consistent with the hypothesis that REM sleep, or a precursor state with aspects of REM sleep, may have had its origin in reptilian species.
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Selected References
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- ASERINSKY E., KLEITMAN N. Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science. 1953 Sep 4;118(3062):273–274. doi: 10.1126/science.118.3062.273. [DOI] [PubMed] [Google Scholar]
- Allison T., Van Twyver H., Goff W. R. Electrophysiological studies of the echidna, Tachyglossus aculeatus. I. Waking and sleep. Arch Ital Biol. 1972 Jul;110(2):145–184. [PubMed] [Google Scholar]
- Allison T., Van Twyver H. Sleep in the moles, Scalopus aquaticus and Condylura cristata. Exp Neurol. 1970 Jun;27(3):564–578. doi: 10.1016/0014-4886(70)90117-2. [DOI] [PubMed] [Google Scholar]
- Ayala-Guerrero F., Huitrón-Reséndiz S. Sleep patterns in the lizard Ctenosaura pectinata. Physiol Behav. 1991 Jun;49(6):1305–1307. doi: 10.1016/0031-9384(91)90369-y. [DOI] [PubMed] [Google Scholar]
- Chase M. H., Morales F. R. The atonia and myoclonia of active (REM) sleep. Annu Rev Psychol. 1990;41:557–584. doi: 10.1146/annurev.ps.41.020190.003013. [DOI] [PubMed] [Google Scholar]
- Emde R. N., Metcalf D. R. An electroencephalographic study of behavioral rapid eye movement states in the human newborn. J Nerv Ment Dis. 1970 May;150(5):376–386. doi: 10.1097/00005053-197005000-00006. [DOI] [PubMed] [Google Scholar]
- Flanigan W. F., Jr, Knight C. P., Hartse K. M., Rechtschaffen A. Sleep and wakefulness in chelonian reptiles. I. The box turtle, Terrapene carolina. Arch Ital Biol. 1974 Jul;112(3):227–252. [PubMed] [Google Scholar]
- Flanigan W. F., Jr Sleep and wakefulness in iguanid lizards, Ctenosaura pectinata and Iguana iguana. Brain Behav Evol. 1973;8(6):401–436. doi: 10.1159/000124366. [DOI] [PubMed] [Google Scholar]
- Huntley A. C. Electrophysiological and behavioral correlates of sleep in the desert iguana, Dipsosaurus dorsalis Hallowell. Comp Biochem Physiol A Comp Physiol. 1987;86(2):325–330. doi: 10.1016/0300-9629(87)90338-0. [DOI] [PubMed] [Google Scholar]
- Jouvet-Mounier D., Astic L., Lacote D. Ontogenesis of the states of sleep in rat, cat, and guinea pig during the first postnatal month. Dev Psychobiol. 1970;2(4):216–239. doi: 10.1002/dev.420020407. [DOI] [PubMed] [Google Scholar]
- Kushida C. A., Bergmann B. M., Rechtschaffen A. Sleep deprivation in the rat: IV. Paradoxical sleep deprivation. Sleep. 1989 Feb;12(1):22–30. doi: 10.1093/sleep/12.1.22. [DOI] [PubMed] [Google Scholar]
- Lai Y. Y., Siegel J. M. Pontomedullary glutamate receptors mediating locomotion and muscle tone suppression. J Neurosci. 1991 Sep;11(9):2931–2937. doi: 10.1523/JNEUROSCI.11-09-02931.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marks G. A., Shaffery J. P. A preliminary study of sleep in the ferret, Mustela putorius furo: a carnivore with an extremely high proportion of REM sleep. Sleep. 1996 Feb;19(2):83–93. doi: 10.1093/sleep/19.2.83. [DOI] [PubMed] [Google Scholar]
- McGinty D., Szymusiak R. Keeping cool: a hypothesis about the mechanisms and functions of slow-wave sleep. Trends Neurosci. 1990 Dec;13(12):480–487. doi: 10.1016/0166-2236(90)90081-k. [DOI] [PubMed] [Google Scholar]
- Nitz D., Siegel J. GABA release in the dorsal raphe nucleus: role in the control of REM sleep. Am J Physiol. 1997 Jul;273(1 Pt 2):R451–R455. doi: 10.1152/ajpregu.1997.273.1.R451. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pivik R. T., Sircar S., Braun C. Nuchal muscle tonus during sleep, wakefulness and tonic immobility in the rabbit. Physiol Behav. 1981 Jan;26(1):13–20. doi: 10.1016/0031-9384(81)90072-x. [DOI] [PubMed] [Google Scholar]
- Rechtschaffen A., Bergmann B. M., Everson C. A., Kushida C. A., Gilliland M. A. Sleep deprivation in the rat: X. Integration and discussion of the findings. Sleep. 1989 Feb;12(1):68–87. [PubMed] [Google Scholar]
- Roffwarg H. P., Muzio J. N., Dement W. C. Ontogenetic development of the human sleep-dream cycle. Science. 1966 Apr 29;152(3722):604–619. doi: 10.1126/science.152.3722.604. [DOI] [PubMed] [Google Scholar]
- Sakai K., Koyama Y. Are there cholinergic and non-cholinergic paradoxical sleep-on neurones in the pons? Neuroreport. 1996 Nov 4;7(15-17):2449–2453. doi: 10.1097/00001756-199611040-00009. [DOI] [PubMed] [Google Scholar]
- Siegel J. M. Behavioral functions of the reticular formation. Brain Res. 1979 Jul;180(1):69–105. doi: 10.1016/0165-0173(79)90017-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegel J. M., Manger P. R., Nienhuis R., Fahringer H. M., Pettigrew J. D. The echidna Tachyglossus aculeatus combines REM and non-REM aspects in a single sleep state: implications for the evolution of sleep. J Neurosci. 1996 May 15;16(10):3500–3506. doi: 10.1523/JNEUROSCI.16-10-03500.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegel J. M., McGinty D. J. Pontine reticular formation neurons: relationship of discharge to motor activity. Science. 1977 May 6;196(4290):678–680. doi: 10.1126/science.193185. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steriade M., McCormick D. A., Sejnowski T. J. Thalamocortical oscillations in the sleeping and aroused brain. Science. 1993 Oct 29;262(5134):679–685. doi: 10.1126/science.8235588. [DOI] [PubMed] [Google Scholar]