Noradrenaline involvement in basic and higher integrated REM sleep processes
Section snippets
Preamble
We were not exactly friends, but we had a friendly relationship. I invited Jean-Michel Gaillard several times to lecture to my students in Nice, and I often traveled to his annual January sleep seminar in Geneva, where I was always impressed by his ability to acutely and kindly discuss each basic neurobiological or psychophysiological result presented by the participants working on animals or humans. I also taught at Abidjan University (Ivory Coast), and once when a student in my laboratory
Results
In this review, I will first analyze all of the papers that have addressed the involvement of NA in basic REM sleep processes. All individual papers have been analyzed based on their full text, and abstracts were almost never taken into account alone. Only the data strictly related to the topic are reported. In Section 4, I will outline our present-day knowledge in this field and then analyze the involvement of NA in the higher integrated brain processes of REM sleep. Since the initial
Noradrenaline involvement in basic REM sleep mechanisms (Table 4)
The most generally accepted idea concerning the relationship between NA and REM sleep is that the locus coeruleus must be silent for this sleep stage to occur. Hence, this neuromodulator must be absent. The most recent model, proposed by Mallick et al. (2005), postulates that during waking REM sleep-off neurons are activated by waking-inducing structures (Mallick et al., 1998, Thankachan et al., 2001) that trigger NA release. The REM sleep-on neurons of the laterodorsal/pedunculopontine
Conclusion
Noradrenaline is crucial for the basic processes of REM sleep. The precise mechanism by which a small amount of this essential neuromodulator is available and acts is still open to discussion. Moreover, the fact that NA, in the classic REM sleep-off neuromodulator model, does not modify REM sleep when infused into the REM sleep-on pedunculopontine tegmentum, also needs to be explained (Datta et al., 2003), as do the results raising questions about its true function in REM sleep-generating and
Acknowledgement
I gratefully thank the referees for helpful suggestions and Dr. Peter Follette for improvement of the English.
References (404)
- et al.
Uncompetitive stimulation of rat brain Na–K ATPase activity by rapid eye movement deprivation
Neurochem. Int.
(2000) - et al.
Evidence for norepinephrine-mediated collateral inhibition of locus coeruleus neurons
Brain. Res.
(1977) - et al.
5-Hydroxytryptamine 2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in the association cortex
Neuroscience
(1991) - et al.
The alpha-1 adrenergic agonist, cirazoline, impairs spatial working memory in aged monkeys
Pharmacol. Biochem. Behav.
(1997) - et al.
Neurobiology of executive functions: catecholamine influences on prefrontal cortical functions
Biol. Psychiat.
(2005) - et al.
Alpha-1noradrenergic receptor stimulation impairs prefrontal cortical cognitive function
Biol. Psychiat.
(1999) - et al.
Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology
Prog. Brain Res.
(1991) - et al.
The interaction between sleep and thermoregulation in adults and neonates
Sleep Med. Rev.
(2002) - et al.
Effects of rapid depletion of phenylalanine and tyrosine on sleep and behavior
Pharmacol. Biochem. Behav.
(1976) - et al.
REM sleep deprivation increases the levels of tyrosine hydroxylase and norepinephrine transporter mRNA in the locus coeruleus
Mol. Brain Res.
(1998)
Synergic sedative effects of noradrenergic alpha(1)- and beta-receptor blockade on forebrain electroencephalographic and behavior indices
Neuroscience
The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes
Brain Res. Rev.
Effects of locus coeruleus inactivation on electroencephalographic activity in neocortex and hippocampus
Neuroscience
Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function
Biol. Psychiat.
Post-pubertal adrenergic changes in rats with neonatal lesions of the ventral hippocampus
Neuropharmacology
REM-enhancing effects of the adrenergic antagonist idazoxan infused into the medial pontine reticular formation of the freely moving cat
Brain Res.
Network reset: a simplified overarching theory of locus coeruleus noradrenaline function
Trends Neurosci.
Fast fronto-parietal rhythms during combined focused attentive behavior and immobility in cat: cortical and thalamic localizations
Electroenceph. Clin. Neurophysiol.
Effects of locus coeruleus lesions upon sleeping and waking in the rabbit
Brain Res.
Evidence for a compromised dorsolateral prefrontal cortical parallel circuit in schizophrenia
Brain Res. Rev.
The mysterious trace amines: protean neuromodulators of synaptic transmission in mammalian brain
Prog. Neurobiol.
Unilateral lesions in locus coeruleus area enhance paradoxical sleep
Electroenceph. Clin. Neurophysiol.
Neuronal firing in the nucleus accumbens is associated with the level of cortical arousal
Neuroscience
Gamma EEG dynamics in neocortex and hippocampus during human wakefulness and sleep
Neuroimage
Modulatory effects of norepinephrine, acting on alpha 1 receptors in the central nucleus of the amygdala, on behavioral and neuroendocrine response to acute immobilization stress
Neuropharmacology
Alterations in the sleep–waking cycle induced by cooling of the locus coeruleus area
Electroenceph. Clin. Neurophysiol.
Effect of noradrenergic denervation of the amygdala upon recovery after sleep deprivation in the rat
Neurosci. Lett.
Effect of noradrenergic denervation of medial prefrontal cortex and dentate gyrus on recovery after sleep deprivation in the rat
Neurosci. Lett.
Locus coeruleus activation by foot shock or electrical stimulation inhibits amygdala neurons
Neuroscience
Subtotal destruction of central noradrenergic projections increases the firing rate of locus coeruleus cells
Brain Res.
Origin of noradrenergic afferents to the shell subregion of the nucleus accumbens: anterograde and retrograde tract-tracing studies in the rat
Brain Res.
The occurrence of low voltage fast electroencephalogram patterns during behavioral sleep in the cat
Electroenceph. Clin. Neurophysiol.
Diffuse regulation of visual thalamo-cortical responsiveness during sleep and wakefulness
Electroenceph. Clin. Neurophysiol.
Noradrenergic axon terminals in the cerebral cortex of rats. III. Topometric ultrastructural analysis
Brain Res.
Pattern of rapid-eye-movement sleep episode occurrence after an immobilization stress in the rat
Neurosci. Lett.
A potent excitatory input to the locus coeruleus from the ventrolateral medulla
Neurosci. Lett.
Two physiologically distinct populations of neurons in the ventrolateral medulla innervate the locus coeruleus
Brain Res.
Potent inhibitory input to the locus coeruleus from the nucleus prepositus hypoglossi
Brain Res. Bull.
Effects of putative neurotransmitters on neuronal activity on monkey auditory cortex
Brain Res.
High-frequency components of the rat electrocorticogram are modulated by the vigilance states
Neurosci. Lett.
The action of noradrenaline on cortical neurons: effects of pH
Brain Res.
The role of norepinephrine in the physiopathology of cognitive disorders: potential applications to the treatment of cognitive dysfunction in schizophrenia and Alzheimer's disease
Biol. Psychiat.
Partial injury to central noradrenergic neurons: reduction of tissue norepinephrine content is greater than reduction of extracellular norepinephrine measured by microdialysis
Neuroscience
Prefrontal DA transmission at D1 receptors and the pathology of schizophrenia
Neuroscientist
Recovery cycles of primary evoked potentials in cats sensorimotor cortex
Experentia
Catecholamine regulation of the prefrontal cortex
J. Psychopharmacol.
Methylphenidate improves prefrontal cortical cognitive function through alpha2 adrenoceptor and dopamine D1 receptor actions: relevance to therapeutic effects in attention deficit hyperactivity disorder
Behav. Brain Funct.
Noradrenergic mechanisms in age-related cognitive deficit
J. Neural Transm. Suppl.
Regularly occurring periods of eye motility, and concomitant phenomena during sleep
Science
Activity of norepinephrine-containing neurons in behaving rats anticipates fluctuations in the sleep–waking cycle
J. Neurosci.
Cited by (26)
The α<inf>1</inf> adrenoceptor antagonist prazosin enhances sleep continuity in fear-conditioned Wistar-Kyoto rats
2014, Progress in Neuro-Psychopharmacology and Biological PsychiatryCitation Excerpt :However, given that locus coeruleus cell firing is thought to be near zero during REMS (and postsynaptic noradrenergic “tone” presumably very low or absent), the question arises how an adrenoceptor antagonist could promote REMS continuity. The explanation may be that just before and very early in an REMS episode, following FC, intrasynaptic NE is present, owing, probably, to the few remaining spikes in locus coeruleus neurons (Gottesmann, 2008). Another possible explanation is that an excitatory glutamatergic input from ventrolateral medullary adrenergic (C1) neurons drives noradrenergic locus coeruleus neurons during REMS in fear-conditioned WKY rats (Abbott et al., 2012).
Activation of inactivation process initiates rapid eye movement sleep
2012, Progress in NeurobiologyCitation Excerpt :However, one study in rabbits suggested that LC may not be essential for REMS, although it may be necessary for sleep integrity and for motor control during sleep (Braun and Pivik, 1981). The necessity of NA for priming and initiation of REMS has also been indicated by other studies (Gaillard, 1983; Gottesmann, 2008; Mallick et al., 2005b). The differences in results are possibly due to variations in methods used in the studies, the extent and types of neurons and/or fibres of passage in LC damaged or stimulated and partly due to lack of information on input and output to and from the damaged neurons and their neurotransmitter type.
The impact of increasing sleep restriction on cortisol and daytime sleepiness in adolescents
2012, Neuroscience LettersCitation Excerpt :Finally, our observations might indicate that cortisol levels are not a very reliable measure to assess the effects of short-term sleep restriction. The repeatedly demonstrated adverse health effects of sleep restriction and sleep loss might be mediated by a broad variety of other pathways, beyond effects on the hypothalamic–pituitary–adrenal axis, such as the noradrenergic system [13,22]. In conclusion, the current findings suggest that short periods of moderate sleep restriction associated with increased daytime sleepiness are not sufficient to significantly increase cortisol levels in healthy adolescents.
REM sleep loss increases brain excitability: Role of noradrenalin and its mechanism of action
2011, Sleep Medicine ReviewsCitation Excerpt :Continuous activation of the NA-ergic neurons by electrical stimulation25,26 or chemical intervention,27,105,106 in an attempt not to allow those neurons to cease firing, has been shown to prevent generation of REMS. Although some NA may prime the system for REMS generation,107,108 based on the findings mentioned above and other supportive evidence, it was proposed that cessation of the NA-ergic REM-OFF neurons is a prerequisite for REMS generation (reviewed in Refs.107–109). Neurons mediate their actions by releasing neurotransmitters; therefore, continuous activity of neurons would cause a sustained release of neurotransmitter stored in them at the projection sites.
Locus Coeruleus and Norepinephrine
2010, Encyclopedia of Movement Disorders, Three-Volume SetLocus Coeruleus and Norepinephrine
2010, Encyclopedia of Movement Disorders