Breathing and brain state: Urethane anesthesia as a model for natural sleep☆
Section snippets
Sleep: a dynamic brain process
Sleep is a fundamental and necessary process with a strong circadian rhythm. Sleep, however, is not a unitary process. It exhibits dynamics expressed most prominently as alternations of brain state that can be measured by local or even more global field potential (LFP/EEG) recordings of brain activity which define the sleep cycle. Most important in the context of this review, respiratory control is significantly modulated in concert with changes in brain state during sleep and this has
Anesthesia: a pharmacological parallel to sleep?
Although sleep is the most common metaphor used for anesthesia by physicians and laypersons alike (Shafer, 1995), it is generally accepted that, aside from the loss of consciousness, reduced sensory awareness, and reduction in behavioral responsiveness, typical anesthesia is divergent from sleep; it is imposed by circulating drugs, it suppresses spontaneous arousal, and most importantly, does not allow the cyclical variability of brain states that typifies natural sleep (Tung and Mendelson, 2004
EEG characteristics under urethane anesthesia
Typical brain state alternations occurring at the level of neocortex (nCTX) and hippocampus (HPC) under urethane anesthesia are displayed in Fig. 1. Local field potentials recorded at level of the nCTX (layer V) and the HPC (pyramidal cell layer) display regular alternations between a state characterized by high amplitude, low frequency activity in the nCTX and HPC (with a peak of activity in the range of ∼1 Hz), and a state characterized by low amplitude, high frequency activity in the HPC in
Respiratory characteristics under urethane anesthesia
Breathing is strongly correlated with brain state, and during sleep, as in wakefulness, breathing is under strong metabolic control. In humans, the early stages of non-REM sleep at sleep onset are characterized by breathing patterns that show very little change in frequency but very irregular tidal volumes, that often result in periodic breathing (oscillations in amplitude) (Krieger, 2005). With progression of sleep into deep non-REM sleep (characterized by the typical cortical SWS) breathing
Factors influencing brain state alternations under urethane anesthesia
While most anesthetics produce a relatively uniform level of anesthesia and brain activity with complete suppression of postural tone, urethane is unique in that spontaneous brain state alternations still occur under a constant level of anesthesia, and postural tone changes, although weak, can be detected across states (Clement et al., 2008). Despite the robust demonstration of spontaneous brain state transitions under urethane anesthesia and parallel changes in multiple physiological systems,
Validity of urethane anesthesia as a model of sleep
How good a model of natural sleep is the urethane anesthetized experimental preparation? Is it useful for studying sleep-related state-dependent modulation of breathing? First, it has to be noted that urethane anesthesia does not completely replicate natural sleep. Urethane anesthetized rodents lack the ability to spontaneously rouse from anesthesia. REM-like states also lack the phasic component of REM sleep, and, as seen with other anesthetics, urethane anesthetized rodents lack central
Acknowledgements
Supported by Canadian Institute of Health Research (GDF, CTD), Women and Children Health Research Institute (GDF, SP), Alberta Lung Association (GDF), Natural Science and Engineering Research Council of Canada (CTD), Parker B. Francis Foundation (SP). GDF and CTD are Alberta Innovates Health Solutions funded investigators.
References (81)
- et al.
Extrinsic and intrinsic properties underlying oscillation and synchrony in limbic cortex
Progress in Neurobiology
(1993) Respiratory chemoreflexes and effects of cortical activation state in urethane anesthetized rats
Respiratory Physiology & Neurobiology
(2004)Sleep under extreme environments: effects of heat and cold exposure, altitude, hyperbaric pressure and microgravity in space
Journal of the Neurological Sciences
(2007)- et al.
Normal Human Sleep: An Overview, Principles and Practice of Sleep Medicine
(2005) - et al.
Congenital central hypoventilation syndrome: not just another rare disorder
Paediatric Respiratory Reviews
(2004) Carbachol in the pontine reticular formation of C57BL/6J mouse decreases acetylcholine release in prefrontal cortex
Neuroscience
(2004)- et al.
Activity of identified cortically projecting and other basal forebrain neurones during large slow waves and cortical activation in anaesthetized rats
Brain Research
(1987) - et al.
Central respiratory pauses, sighs, and gross body movements during sleep in children
Physiology & Behavior
(2004) The impact of sleep deprivation on neuronal and glial signaling pathways important for memory and synaptic plasticity
Cellular Signalling
(2012)Neuromodulation of hypoglossal motoneurons during sleep
Respiratory Physiology & Neurobiology
(2008)
Cortical activation states in sleep and anesthesia. II: respiratory reflexes
Respiration Physiology
Cortical activation states in sleep and anesthesia. I: Cardio-respiratory effects
Respiration Physiology
Respiratory Physiology: Breathing in Normal Subjects, Principles and Practice of Sleep Medicine
Respiratory roles of genioglossus, sternothyroid, and sternothyroid muscles during sleep
Experimental Neurology
State-dependent sensory gating in olfactory cortex
Neuron
Comparative metabolism and disposition of ethyl carbamate (urethane) in male Fischer 344 rats and male B6C3F1 mice
Toxicology and Applied Pharmacology
Respiratory Physiology: Central Neural Control, Principles and Practice of Sleep Medicine
Rapid eye movement sleep induction by microinjection of the GABA-A antagonist bicuculline into the dorsal subcoeruleus area of the rat
Brain Research
Maturation of breathing
Clinics in Perinatology
Two types of cerebral activation during active sleep: relations to behavior
Brain Research
Disturbances in cardiorespiratory function during day and night in Rett syndrome
Pediatric Neurology
Fos expression in pontomedullary catecholaminergic cells following rapid eye movement sleep-like episodes elicited by pontine carbachol in urethane-anesthetized rats
Neuroscience
The human tongue during sleep: electromyographic activity of the genioglossus muscle
Experimental Neurology
Respiratory EMG activity of the posterior cricoarytenoid, cricothyroid and diaphragm muscles during sleep
Respiration Physiology
Sleep influences on diaphragmatic motor unit discharge
Experimental Neurology
Locus coeruleus neuronal activity during the sleep–waking cycle in mice
Neuroscience
Anesthetics and control of breathing
Respiratory Physiology & Neurobiology
Anesthesia and sleep
Sleep Medicine Reviews
Sleep patterns of five rodent species
Physiology & Behavior
Cerebral activity and behavior: control by central cholinergic and serotonergic systems
International Review of Neurobiology
State-dependent functional connectivity of rat olfactory system assessed by fMRI
Neuroscience Letters
Mammalian Sleep, Principles and Practice of Sleep Medicine
Sleep regulation in rats during early development
American Journal of Physiology
Main trends in rectal temperature during sleep. Hypnogram and thermogram
Neuropsychobiology
How do general anaesthetics work?
Naturwissenschaften
Periodic respiratory pattern occurring in conjunction with eye movements during sleep
Science
Regularly occurring periods of eye motility, and concomitant phenomena, during sleep
Science
Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep–waking cycle
Journal of Neuroscience
Maturation of fetal breathing activity
Biology of the Neonate
Control of sleep and wakefulness
Physiological Reviews
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Modulation of Spontaneous and Light-Induced Activity in the Rat Dorsal Lateral Geniculate Nucleus by General Brain State Alterations under Urethane Anesthesia
2019, NeuroscienceCitation Excerpt :and ‘SWA’ abbreviations were used, which refer to cortical activation and cortical slow wave activity phases of urethane sleep, respectively. Although, they should not be confused with natural sleep stages, several studies emphasised that activation and SWA alternations of urethane naesthesia are valid and commonly used model of natural sleep (Clement et al., 2008; Blasiak et al., 2013; Pagliardini et al., 2013a,b). ECoG signals containing both activated and SWA phases (650 s long recordings, one alteration in ECoG) were subjected to discrete Fast Fourier Transform with the Hann window function.
Neurobiological Parallels, Overlaps, and Divergences of Sleep and Anesthesia
2019, Handbook of Behavioral NeuroscienceCitation Excerpt :Physiological activity in REM sleep can further be dissociated into two subcategories: tonic features, which are primarily composed of the archetypical REM-induced muscle atony, and phasic features, which are composed of the hallmark rapid saccadic eye movements of REM and muscle twitches in both extremities and middle ear muscles (Aserinsky, 1965; Mashour & Pal, 2012; Rechtschaffen & Siegel, 2000). Both tonic and phasic events occur in a typical REM epoch (Pagliardini, Funk, et al., 2013). All other sleep falls under the broad classification of non-REM (NREM) sleep, which is a state characterized by high-voltage, low-frequency electrophysiological activity (Rechtschaffen & Siegel, 2000).
The Modulation by Anesthetics and Analgesics of Respiratory Rhythm in the Nervous System
2024, Current Neuropharmacology
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This paper is part of a special issue entitled “Sleep and Breathing” guest-edited by Dr. James Duffin, Dr. Leszek Kubin and Dr. Jason Mateika.