Slow waves, sharp waves, ripples, and REM in sleeping dragons

Shein-Idelson, Mark; Ondracek, Janie M.; Liaw, Hua-Peng; Reiter, Sam; Laurent, Gilles

doi:10.1126/science.aaf3621

Cited by 194 publications

(194 citation statements)

References 48 publications

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“…Whereas the reptilian hippocampus possesses many fewer recognizable areas than that of mammals, the significance of this difference is at present unknown. It is our hope that, by combining modern anatomical, molecular, and electrophysiological techniques in multiple reptilian species [Shein-Idelson et al, 2016, 2017Tosches et al, in preparation], important questions concerning cortex and hippocampal evolution and function will be answered. Doody JS, Burghardt GM, Dinets V (2013) …”

Section: Discussionmentioning

confidence: 99%

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

Reiter

Liaw²,

Yamawaki³

et al. 2017

Brain Behav Evol

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Our ability to navigate through the world depends on the function of the hippocampus. This old cortical structure plays a critical role in spatial navigation in mammals and in a variety of processes, including declarative and episodic memory and social behavior. Intense research has revealed much about hippocampal anatomy, physiology, and computation; yet, even intensely studied phenomena such as the shaping of place cell activity or the function of hippocampal firing patterns during sleep remain incompletely understood. Interestingly, while the hippocampus may be a ‘higher order' area linked to a complex cortical hierarchy in mammals, it is an old cortical structure in evolutionary terms. The reptilian cortex, structurally much simpler than the mammalian cortex and hippocampus, therefore presents a good alternative model for exploring hippocampal function. Here, we trace common patterns in the evolution of the hippocampus of reptiles and mammals and ask which parts can be profitably compared to understand functional principles. In addition, we describe a selection of the highly diverse repertoire of reptilian behaviors to illustrate the value of a comparative approach towards understanding hippocampal function.

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Section: Discussionmentioning

confidence: 99%

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

Reiter

Liaw²,

Yamawaki³

et al. 2017

Brain Behav Evol

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“…Sleep is found to be universal in all animals studied, 37 essential to life, 38,39 and important to development 40,41 ; yet there are reports of constant locomotion behaviors in dolphins, 42 whale calves, 43 and migrating birds. 44 Although these studies do not show electrophysiological evidence of sleep, some authors posit that unihemispheric sleep is likely 45,46 and that migratory birds must somehow sleep in flight.…”

Section: Broader Implications Of the Findingsmentioning

confidence: 99%

Different Simultaneous Sleep States in the Hippocampus and Neocortex

Emrick

Gross

Riley

et al. 2016

Sleep

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Study Objectives: Investigators assign sleep-waking states using brain activity collected from a single site, with the assumption that states occur at the same time throughout the brain. We sought to determine if sleep-waking states differ between two separate structures: the hippocampus and neocortex. Methods: We measured electrical signals (electroencephalograms and electromyograms) during sleep from the hippocampus and neocortex of five freely behaving adult male rats. We assigned sleep-waking states in 10-sec epochs based on standard scoring criteria across a 4-h recording, then analyzed and compared states and signals from simultaneous epochs between sites. Results: We found that the total amount of each state, assigned independently using the hippocampal and neocortical signals, was similar between the hippocampus and neocortex. However, states at simultaneous epochs were different as often as they were the same (P = 0.82). Furthermore, we found that the progression of states often flowed through asynchronous state-pairs led by the hippocampus. For example, the hippocampus progressed from transitionto-rapid eye movement sleep to rapid eye movement sleep before the neocortex more often than in synchrony with the neocortex (38.7 ± 16.2% versus 15.8 ± 5.6% mean ± standard error of the mean). Conclusions: We demonstrate that hippocampal and neocortical sleep-waking states often differ in the same epoch. Consequently, electrode location affects estimates of sleep architecture, state transition timing, and perhaps even percentage of time in sleep states. Therefore, under normal conditions, models assuming brain state homogeneity should not be applied to the sleeping or waking brain.

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“…Birds and nonavian reptiles are members of the Sauropsida whereas mammals are members of Synapsida, clades that last shared a common ancestor over 300 million years ago. Whether the presence of SWS and REM sleep in such evolutionarily distant groups is the result of convergent evolution or these states were present in, and inherited from, a common ancestor is still a subject of debate [Libourel and Herrel, 2015;Shein-Idelson et al, 2016]. Obviously, studies of the sleep patterns of nonavian reptiles and the anamniote out-group to amniotes (amphibians) are required to resolve this question.…”

Section: Evolution Of Sws and Rem Sleep: Convergence Or Inheritance?mentioning

confidence: 99%

“…Behaviors suggestive of REM sleep, including eye movements under closed eyelids and myoclonic twitches, have been observed across a variety of reptilian groups, in some cases accompanied by wake-like EEG activity [Tauber et al, 1966;Ayala-Guerrero and Vargas Reyna, 1987;Ayala-Guerrero et al, 1988;Shein-Idelson et al, 2016;reviewed in Hartse, 1994;Libourel and Herrel, 2015]. However, because arousal thresholds were not assessed during these periods, it remains unclear whether they reflect REM sleep or partial awakenings [Hartse, 1994;Libourel and Herrel, 2015;Shein-Idelson et al, 2016]. In addition, several studies in lizards, turtles, and crocodilians have not found REM sleep [Hartse, 1994;Eiland et al, 2001;Libourel and Herrel, 2015].…”

Section: Evolution Of Sws and Rem Sleep: Convergence Or Inheritance?mentioning

confidence: 99%

“…A common (albeit not universal) electrophysiological correlate of behavioral sleep in reptiles is intermittent high-voltage sharp waves (HVS) in the reptilian cortex and the dorsal ventricular ridge [Hartse, 1994;Shein-Idelson et al, 2016]. Several investigators have suggested that HVS reflect neural activity comparable to that occurring in the mammalian hippocampus during SWS [Hartse, 1994;Shein-Idelson et al, 2016], whereas others have suggested that HVS are homologous in some respects to SWS-related slow waves [Rattenborg and Martinez-Gonzalez, 2014]. Despite these different opinions, most researchers agree that HVS occur during a state homologous to SWS in mammals and birds.…”

Section: Evolution Of Sws and Rem Sleep: Convergence Or Inheritance?mentioning

confidence: 99%

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Sleep-Related Electrophysiology and Behavior of Tinamous (<b><i>Eudromia elegans</i></b>): Tinamous Do Not Sleep Like Ostriches

Tisdale¹,

Vyssotski²,

Lesku³

et al. 2017

Brain Behav Evol

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The functions of slow wave sleep (SWS) and rapid eye movement (REM) sleep, distinct sleep substates present in both mammals and birds, remain unresolved. One approach to gaining insight into their function is to trace the evolution of these states through examining sleep in as many taxonomic groups as possible. The mammalian and avian clades are each composed of two extant groups, i.e., the monotremes (echidna and platypus) and therian (marsupial and eutherian [or placental]) mammals, and Palaeognaths (cassowaries, emus, kiwi, ostriches, rheas, and tinamous) and Neognaths (all other birds) among birds. Previous electrophysiological studies of monotremes and ostriches have identified a unique “mixed” sleep state combining features of SWS and REM sleep unlike the well-delineated sleep states observed in all therian mammals and Neognath birds. In the platypus this state is characterized by periods of REM sleep-related myoclonic twitching, relaxed skeletal musculature, and rapid eye movements, occurring in conjunction with SWS-related slow waves in the forebrain electroencephalogram (EEG). A similar mixed state was also observed in ostriches; although in addition to occurring during periods with EEG slow waves, reduced muscle tone and rapid eye movements also occurred in conjunction with EEG activation, a pattern typical of REM sleep in Neognath birds. Collectively, these studies suggested that REM sleep occurring exclusively as an integrated state with forebrain activation might have evolved independently in the therian and Neognath lineages. To test this hypothesis, we examined sleep in the elegant crested tinamou (Eudromia elegans), a small Palaeognath bird that more closely resembles Neognath birds in size and their ability to fly. A 24-h period was scored for sleep state based on electrophysiology and behavior. Unlike ostriches, but like all of the Neognath birds examined, all indicators of REM sleep usually occurred in conjunction with forebrain activation in tinamous. The absence of a mixed REM sleep state in tinamous calls into question the idea that this state is primitive among Palaeognath birds and therefore birds in general.

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Slow waves, sharp waves, ripples, and REM in sleeping dragons

Cited by 194 publications

References 48 publications

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

Different Simultaneous Sleep States in the Hippocampus and Neocortex

Sleep-Related Electrophysiology and Behavior of Tinamous (<b><i>Eudromia elegans</i></b>): Tinamous Do Not Sleep Like Ostriches

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