Arousal threshold in the cat as a function of sleep phase and stimulus significance

Siegel, Jerome H.; Langley, Th. D.

doi:10.1007/bf02138511

Cited by 29 publications

(24 citation statements)

References 5 publications

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“…For one thing, our data show an altered distribution of firing rates which could throw off any simple read-out by higher cortical areas such as association areas or frontal cortex (if read-out mechanisms are even online during sleep). Assuming A1 and LB play a role in perception during sleep, our data suggest that information carried by mean activity levels or temporal response patterns may reflect the neural basis for subconscious detection or discrimination of sounds during sleep in humans (Bonnet, 1982; Oswald et al, 1960; Beh and Barrat, 1965; Langford et al, 1974; McDonald et al, 1975; Voss and Harsh, 1998) and animals (Halperin and Iorio, 1981; Siegel and Langley, 1965; Van Twyver and Garrett, 1972; Maho and Hennevin, 1999). The findings reported here stand in contrast to original theories that assumed that the brain shuts off to the external world during sleep (Steriade et al, 2003a).…”

Section: Discussionmentioning

confidence: 83%

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: 83%

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Issa¹,

Wang²

2008

J. Neurosci.

113

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“…Some studies in other sleep models have reported differences in arousability from different sleep stages, and while REM sleep was originally hypothesized to be associated with increased vigilance, this has not been confirmed experimentally (Siegel and Langley, 1965; Snyder, 1966). In the current dog studies, the PSG analyses indicated that vehicle- and DORA-treated dogs were similarly able to awaken from all sleep stages in response to the conditioned acoustic stimulus, without a predictive effect of sleep stage on arousability.…”

Section: Discussionmentioning

confidence: 99%

“…It has been established that the emotional significance of a stimulus is associated with the ability to induce an arousal response from natural sleep, as demonstrated by early sleep experiments in rodents (Van Twyver and Garrett, 1972), cats (Buendia et al, 1963; Siegel and Langley, 1965), and humans (Oswald et al, 1960; Langford et al, 1974). Consistent with the historical literature, the DORA- and vehicle-treated dogs in this study awoke completely in response to the emotionally salient conditioned tone presentation but were not aroused by similar tones played randomly without conditioning.…”

Section: Discussionmentioning

confidence: 99%

“…Video recordings during the arousal testing subjectively confirmed animal excitation upon presentation of the salient stimulus during both the vehicle and DORA trials. Meanwhile, the predominant use of negatively conditioned stimuli in studies of salience gated arousal in natural sleep in the historical animal literature (Buendia et al, 1963; Siegel and Langley, 1965; Van Twyver and Garrett, 1972) gives confidence that negative stimuli may also be associated with differential increases in arousal during DORA-induced somnolence.…”

Section: Discussionmentioning

confidence: 99%

“…Classic studies in sleeping animals demonstrated that the threshold for awakening to emotionally relevant acoustic stimuli is much lower than the threshold for waking to an irrelevant auditory stimulus (Buendia et al, 1963; Dillon and Webb, 1965; Siegel and Langley, 1965; Van Twyver and Garrett, 1972; Langford et al, 1974; Halperin and Iorio, 1981; Coenen, 2010). Early laboratory studies involving the presentation of negatively conditioned acoustic stimuli, such as a tone associated with a shock, found animals more likely to awaken to these relevant conditioned versus neutral acoustic stimuli (Buendia et al, 1963; Van Twyver and Garrett, 1972; Halperin and Iorio, 1981).…”

Section: Introductionmentioning

confidence: 99%

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Orexin receptor antagonist-induced sleep does not impair the ability to wake in response to emotionally salient acoustic stimuli in dogs

Tannenbaum

Stevens

Binns

et al. 2014

Front. Behav. Neurosci.

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The ability to awaken from sleep in response to important stimuli is a critical feature of normal sleep, as is maintaining sleep continuity in the presence of irrelevant background noise. Dual orexin receptor antagonists (DORAs) effectively promote sleep across species by targeting the evolutionarily conserved wake-promoting orexin signaling pathway. This study in dogs investigated whether DORA-induced sleep preserved the ability to awaken appropriately to salient acoustic stimuli but remain asleep when exposed to irrelevant stimuli. Sleep and wake in response to DORAs, vehicle, GABA-A receptor modulators (diazepam, eszopiclone and zolpidem) and antihistamine (diphenhydramine) administration were evaluated in telemetry-implanted adult dogs with continuous electrocorticogram, electromyogram (EMG), electrooculogram (EOG), and activity recordings. DORAs induced sleep, but GABA-A modulators and antihistamine induced paradoxical hyperarousal. Thus, salience gating studies were conducted during DORA-22 (0.3, 1, and 5 mg/kg; day and night) and vehicle nighttime sleep. The acoustic stimuli were either classically conditioned using food reward and positive attention (salient stimulus) or presented randomly (neutral stimulus). Once conditioned, the tones were presented at sleep times corresponding to maximal DORA-22 exposure. In response to the salient stimuli, dogs woke completely from vehicle and orexin-antagonized sleep across all sleep stages but rarely awoke to neutral stimuli. Notably, acute pharmacological antagonism of orexin receptors paired with emotionally salient anticipation produced wake, not cataplexy, in a species where genetic (chronic) loss of orexin receptor signaling leads to narcolepsy/cataplexy. DORA-induced sleep in the dog thereby retains the desired capacity to awaken to emotionally salient acoustic stimuli while preserving uninterrupted sleep in response to irrelevant stimuli.

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Induction of both emotional behavior and a novel form of REm sleep by chemical stimulation applied to cat mesencephalon

Baxter¹

1969

Experimental Neurology

140

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Arousal threshold in the cat as a function of sleep phase and stimulus significance

Cited by 29 publications

References 5 publications

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Sensory Responses during Sleep in Primate Primary and Secondary Auditory Cortex

Orexin receptor antagonist-induced sleep does not impair the ability to wake in response to emotionally salient acoustic stimuli in dogs

Induction of both emotional behavior and a novel form of REm sleep by chemical stimulation applied to cat mesencephalon

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