Neurophysiology of Avian Sleep: Comparing Natural Sleep and Isoflurane Anesthesia

Meij, Jacqueline van der; Martı́nez-González, Dolores; Beckers, Gabriël J. L.; Rattenborg, Niels Christian

doi:10.3389/fnins.2019.00262

Cited by 15 publications

(13 citation statements)

References 56 publications

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“…finches. Similar events have also been described in anesthetized pigeons (24). This evidence for avian SWRs follows similar evidence in sleeping reptiles (13,14) and suggests that the evolutionary origin of large-amplitude, highly synchronous SWR events may have already been present in the stem-amniote ancestor to birds, reptiles, and mammals.…”

Section: Discussionsupporting

confidence: 81%

Hippocampal-like network dynamics underlie avian sharp wave-ripples

Yeganegi

Luksch

Ondracek

2019

Preprint

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Sharp wave ripples (SWR) represent one of the most synchronous population patterns in the mammalian brain. Although SWRs are highly conserved throughout mammalian evolution, the existence of SWRs in non-mammalian species remains controversial. We reexamined the existence of avian SWRs by recording the brain activity during sleep and under anesthesia in two species of birds, the zebra finch and the chicken. Electrophysiological recordings using silicon probes implanted in the avian telencephalon revealed highly dynamic switching between high and low delta phases during sleep. High delta phases were composed of large-amplitude, negative deflections (sharp waves) that coincided with a high frequency oscillation (ripple). Correlation analysis revealed that these events were highly synchronous and spanned a large anatomical range of the avian telencephalon. Finally, detailed spike analysis revealed that an increase in the population spiking activity coincided with the occurrence of SWRs, that this spiking activity occurred in specific sequences of spike patterns locked to the SWRs, and that the mean population spiking activity peaked prior to the trough of the negative deflection. These results provide the first evidence of avian SWRs during natural sleep and under anesthesia, and suggest that the evolutionary origin of SWR activity may precede the mammalian-sauropsid bifurcation.avian sleep | sharp wave-ripples | evolution Correspondence: janie.ondracek@tum.de

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Section: Discussionsupporting

confidence: 81%

Hippocampal-like network dynamics underlie avian sharp wave-ripples

Yeganegi

Luksch

Ondracek

2019

Preprint

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“…The mechanisms that mediate avian slow wave propagation remain unclear. Nonetheless, from multi-electrode recordings of anesthesia-induced slow waves, which in many aspects, including propagation pattern, resemble NREM slow waves (van der Meij et al, 2019b), it is clear that the extracellular depolarization of LFP waves is spatio-temporally closely matched by local action potential activity (Beckers et al, 2014), as is the case during NREM sleep in the human neocortex (Nir et al, 2011). Consequently, propagating slow waves appear to reflect the sequential local activation of neurons in the avian brain.…”

Section: Local Aspects Of Nrem Sleepmentioning

confidence: 99%

Local Aspects of Avian Non-REM and REM Sleep

et al. 2019

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Birds exhibit two types of sleep that are in many respects similar to mammalian rapid eye movement (REM) and non-REM (NREM) sleep. As in mammals, several aspects of avian sleep can occur in a local manner within the brain. Electrophysiological evidence of NREM sleep occurring more deeply in one hemisphere, or only in one hemisphere – the latter being a phenomenon most pronounced in dolphins – was actually first described in birds. Such asymmetric or unihemispheric NREM sleep occurs with one eye open, enabling birds to visually monitor their environment for predators. Frigatebirds primarily engage in this form of sleep in flight, perhaps to avoid collisions with other birds. In addition to interhemispheric differences in NREM sleep intensity, the intensity of NREM sleep is homeostatically regulated in a local, use-depended manner within each hemisphere. Furthermore, the intensity and temporo-spatial distribution of NREM sleep-related slow waves varies across layers of the avian hyperpallium – a primary visual area – with the slow waves occurring first in, and propagating through and outward from, thalamic input layers. Slow waves also have the greatest amplitude in these layers. Although most research has focused on NREM sleep, there are also local aspects to avian REM sleep. REM sleep-related reductions in skeletal muscle tone appear largely restricted to muscles involved in maintaining head posture. Other local aspects of sleep manifest as a mixture of features of NREM and REM sleep occurring simultaneously in different parts of the neuroaxis. Like monotreme mammals, ostriches often exhibit brainstem-mediated features of REM sleep (muscle atonia and REMs) while the hyperpallium shows EEG slow waves typical of NREM sleep. Finally, although mice show slow waves in thalamic input layers of primary sensory cortices during REM sleep, this is not the case in the hyperpallium of pigeons, suggesting that this phenomenon is not a universal feature of REM sleep. Collectively, the local aspects of sleep described in birds and mammals reveal that wakefulness, NREM sleep, and REM sleep are not always discrete states.

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“…Nonetheless, the precise mechanisms by which the general anesthetics cause the sudden reversible loss of consciousness, remain to be pinpointed. The sedative effects of anesthetics such as drowsiness, calmness and reduction of motor tone are behaviorally similar to the features of the non-rapid eye movement (NREM) period of sleep ( Franks and Zecharia, 2011 ; van der Meij et al, 2019 ). Some whole-brain imaging studies have also shown that the states of “unconsciousness” during deep sleep and anesthesia are remarkably similar ( Franks, 2008 ).…”

Section: Introductionmentioning

confidence: 97%

“…Some whole-brain imaging studies have also shown that the states of “unconsciousness” during deep sleep and anesthesia are remarkably similar ( Franks, 2008 ). Moreover, similar slow-wave spatiotemporal properties during NREM sleep and isoflurane anesthesia suggest that both types of slow-waves are based on related processes ( van der Meij et al, 2019 ). Recently, growing evidence proved that general anesthesia-induced unconsciousness and natural sleep shared some neural networks ( Zhong et al, 2017 ; van der Meij et al, 2019 ; Zhang et al, 2019 ; Liu et al, 2020b ).…”

Section: Introductionmentioning

confidence: 99%

Lateral Habenula Glutamatergic Neurons Modulate Isoflurane Anesthesia in Mice

Liu

Zhou

et al. 2021

Front. Mol. Neurosci.

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Since their introduction in the 1840s, one of the largest mysteries of modern anesthesia are how general anesthetics create the state of reversible loss of consciousness. Increasing researchers have shown that neural pathways that regulate endogenous sleep–wake systems are also involved in general anesthesia. Recently, the Lateral Habenula (LHb) was considered as a hot spot for both natural sleep–wake and propofol-induced sedation; however, the role of the LHb and related pathways in the isoflurane-induced unconsciousness has yet to be identified. Here, using real-time calcium fiber photometry recordings in vivo, we found that isoflurane reversibly increased the activity of LHb glutamatergic neurons. Then, we selectively ablated LHb glutamatergic neurons in Vglut2-cre mice, which caused a longer induction time and less recovery time along with a decrease in delta-band power in mice under isoflurane anesthesia. Furthermore, using a chemogenetic approach to specifically activate LHb glutamatergic neurons shortened the induction time and prolonged the recovery time in mice under isoflurane anesthesia with an increase in delta-band power. In contrast, chemogenetic inhibition of LHb glutamatergic neurons was very similar to the effects of selective lesions of LHb glutamatergic neurons. Finally, optogenetic activation of LHb glutamatergic neurons or the synaptic terminals of LHb glutamatergic neurons in the rostromedial tegmental nucleus (RMTg) produced a hypnosis-promoting effect in isoflurane anesthesia with an increase in slow wave activity. Our results suggest that LHb glutamatergic neurons and pathway are vital in modulating isoflurane anesthesia.

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Neurophysiology of Avian Sleep: Comparing Natural Sleep and Isoflurane Anesthesia

Cited by 15 publications

References 56 publications

Hippocampal-like network dynamics underlie avian sharp wave-ripples

Hippocampal-like network dynamics underlie avian sharp wave-ripples

Local Aspects of Avian Non-REM and REM Sleep

Lateral Habenula Glutamatergic Neurons Modulate Isoflurane Anesthesia in Mice

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