Low-threshold neuronal activity of spinal dorsal horn neurons increases during REM sleep in cats: comparison with effects of anesthesia

Kishikawa, Keiji; Uchida, Hiroshi; Yamamori, Yuji; Collins, J. G.

doi:10.1152/jn.1995.74.2.763

Cited by 20 publications

(15 citation statements)

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“…The fact that REM behaved independently from SWS suggests the presence of an independent sleep state with no analog under anesthesia. That the sleep state is different than the anesthetized state with regard to single neurons has been seen elsewhere (Torterolo et al, 2002; Cotillon-Williams et al, 2003; Kishikawa et al, 1995; see review by Hennevin et al, 2007). …”

Section: Discussionmentioning

confidence: 90%

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Issa¹,

Wang²

2008

J. Neurosci.

113

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Most sensory stimuli do not reach conscious perception during sleep. It has been thought that the thalamus prevents the relay of sensory information to cortex during sleep, but the consequences for cortical responses to sensory signals in this physiological state remain unclear. We recorded from two auditory cortical areas downstream of the thalamus in naturally sleeping marmoset monkeys. Single neurons in primary auditory cortex (A1) either increased or decreased their responses during sleep compared to wakefulness. In lateral belt (LB), a secondary auditory cortical area, the response modulation was also bidirectional and showed no clear systematic depressive effect of sleep. When averaged across neurons, sound-evoked activity in these two auditory cortical areas was surprisingly well-preserved during sleep. Neural responses to acoustic stimulation were present during both slow-wave (SWS) and rapid-eye movement (REM) sleep, were repeatedly observed over multiple sleep cycles, and demonstrated similar discharge patterns to the responses recorded during wakefulness in the same neuron. Our results suggest that the thalamus is not as effective a gate for the flow of sensory information as previously thought. At the cortical stage, a novel pattern of activation/deactivation appears across neurons. Since the neural signal reaches as far as secondary auditory cortex, this leaves open the possibility of altered sensory processing of auditory information during sleep.

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Section: Discussionmentioning

confidence: 90%

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Issa¹,

Wang²

2008

J. Neurosci.

113

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“…To date, REMS-related suppression of transmission has been reported for trigeminal sensory pathways and it was explained, at least in part, by a state-dependent primary afferent depolarization [118], [119]. In contrast, activity of dorsal spinocerebellar and spinoreticular tract neurons was reported to be suppressed, increased or unchanged [120], [121], [122], [123], [124], and the tactile receptive fields and tactile responsiveness of a majority of spinal dorsal horn neurons were increased during REMS [125]. The variability of these results may be caused by a convergence on these neurons of possibly opposite effects mediated by central REMS-related pathways and changes in peripheral inputs associated with the atonia of REMS.…”

Section: Discussionmentioning

confidence: 99%

Evidence That Adrenergic Ventrolateral Medullary Cells Are Activated whereas Precerebellar Lateral Reticular Nucleus Neurons Are Suppressed during REM Sleep

et al. 2013

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Rapid eye movement sleep (REMS) is generated in the brainstem by a distributed network of neurochemically distinct neurons. In the pons, the main subtypes are cholinergic and glutamatergic REMS-on cells and aminergic REMS-off cells. Pontine REMS-on cells send axons to the ventrolateral medulla (VLM), but little is known about REMS-related activity of VLM cells. In urethane-anesthetized rats, dorsomedial pontine injections of carbachol trigger REMS-like episodes that include cortical and hippocampal activation and suppression of motoneuronal activity; the episodes last 4–8 min and can be elicited repeatedly. We used this model to determine whether VLM catecholaminergic cells are silenced during REMS, as is typical of most aminergic neurons studied to date, and to investigate other REMS-related cells in this region. In 18 anesthetized, paralyzed and artificially ventilated rats, we obtained extracellular recordings from VLM cells when REMS-like episodes were elicited by pontine carbachol injections (10 mM, 10 nl). One major group were the cells that were activated during the episodes (n = 10). Their baseline firing rate of 3.7±2.1 (SD) Hz increased to 9.7±2.1 Hz. Most were found in the adrenergic C1 region and at sites located less than 50 µm from dopamine β-hydroxylase-positive (DBH+) neurons. Another major group were the silenced or suppressed cells (n = 35). Most were localized in the lateral reticular nucleus (LRN) and distantly from any DBH+ cells. Their baseline firing rates were 6.8±4.4 Hz and 15.8±7.1 Hz, respectively, with the activity of the latter reduced to 7.4±3.8 Hz. We conclude that, in contrast to the pontine noradrenergic cells that are silenced during REMS, medullary adrenergic C1 neurons, many of which drive the sympathetic output, are activated. Our data also show that afferent input transmitted to the cerebellum through the LRN is attenuated during REMS. This may distort the spatial representation of body position during REMS.

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“…Because A5 neurons project to the dorsal horn of the spinal cord, their silencing during REM sleep, along with the silencing of other noradrenergic neurons, may explain the increase in the size of the receptive field of dorsal horn neurons during this state (29).…”

Section: Discussionmentioning

confidence: 99%

A5 cells are silenced when REM sleep-like signs are elicited by pontine carbachol

Fenik

Marchenko

Janssen

et al. 2002

Journal of Applied Physiology

111

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. A5 cells are silenced when REM sleep-like signs are elicited by pontine carbachol. J Appl Physiol 93: 1448-1456, 2002. First published June 14, 2002 10.1152/japplphysiol.00225.2002The A5 noradrenergic neurons are considered important for cardiorespiratory regulation. We hypothesized that A5 cells are silenced during rapid eye movement (REM) sleep, thereby contributing to cardiorespiratory changes and suppression of hypoglossal (XII) motoneuronal activity. We used an anesthetized, paralyzed, and artificially ventilated rat in which pontine microinjections of carbachol trigger signs of REM sleep, including hippocampal theta rhythm, motor suppression, and silencing of locus coeruleus neurons. All 16 putative noradrenergic A5 cells recorded were strongly suppressed when the REM sleep-like episodes were elicited and also after intravenous clonidine. Antidromic mapping showed that none of six neurons tested projected to the XII nucleus, whereas three of five projected to the nucleus of the solitary tract and two of four to the rostral ventrolateral medulla. Bilateral microinjections of clonidine into the A5 regions did not alter XII nerve activity. These data suggest that A5 neurons are silenced during natural REM sleep. This will lead to decreased norepinephrine release and may alter synaptic transmission in the nucleus of the solitary tract and rostral ventrolateral medulla without, however, a detectable impact on XII motoneurons. hypoglossal motoneurons; norepinephrine; nucleus of the solitary tract; pons; rapid eye movement sleep THE NOREPINEPHRINE-CONTAINING neurons of the A5 group, located in the ventrolateral pons between the root of the facial nerve and the superior olive, are considered important regulators of cardiorespiratory function (reviewed in Refs. 11,24,25,45,46). They have extensive axonal projections that include cardiorespiratory and motor regions of the brain stem and spinal cord (1,8,9,23,36). Through these projections, they may control, among others, sympathetic and respiratory outputs and, via projection to the hypoglossal (XII) motor nucleus, may mediate noradrenergic excitation of XII motoneurons (5,22,27,40,49). XII motoneurons are of particular interest because they innervate the genioglossus muscle of the tongue, an important airway dilator. Its decreased activity during sleep contributes, in predisposed individuals, to the pathophysiology of the obstructive sleep apnea syndrome (34).The noradrenergic neurons of the locus coeruleus (LC) and the sub-LC region show a robust relationship of their firing frequency with the sleep-wake cycle: the highest activity occurs during wakefulness, and the lowest during the rapid eye movement (REM) stage of sleep (6,43). Consistent with these findings, the extracellular level of norepinephrine is reduced in the XII nucleus during the motor atonia produced by electrical stimulation of the pontine reticular formation region implicated in the triggering of REM sleep (35). The noradrenergic cells of the A5 group may be similarly modulated with the sleep-wa...

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Low-threshold neuronal activity of spinal dorsal horn neurons increases during REM sleep in cats: comparison with effects of anesthesia

Cited by 20 publications

References 0 publications

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Evidence That Adrenergic Ventrolateral Medullary Cells Are Activated whereas Precerebellar Lateral Reticular Nucleus Neurons Are Suppressed during REM Sleep

A5 cells are silenced when REM sleep-like signs are elicited by pontine carbachol

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