Dolphin continuous auditory vigilance for five days

Ridgway, Sam H.; Carder, Donald A.; Finneran, James J.; Keogh, Mandy; Kamolnick, Tricia; Todd, Mark; Goldblatt, Allen

doi:10.1242/jeb.02405

Cited by 53 publications

(56 citation statements)

References 32 publications

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“…Sleep rebounds are highly variable in vertebrates and invertebrates, rarely meeting the homeostatic requirement of full compensation for sleep loss, and several instances of little or no response have been reported. Examples of the latter include male Drosophila (CS strain) after 6h of mechanical stimulation (Huber et al, 2004), zebrafish (Danio rerio) after 6h or 3 days of light-induced vigilance (Yokogawa et al, 2007), pigeons (Columba livia) following light-induced sleep deprivation (Tobler and Borbely, 1988;Berger and Phillips, 1994), golden-mantled ground squirrels (Spermophilus lateralis) following 3h of gentle handling during the post-hibernation period (Larkin and Heller, 1998), squirrel monkeys (Saimiri sciureus) following up to 36h of mild disturbance (Klerman et al, 1999), bottlenose dolphins (Tursiops truncates) following up to 5 days of auditory vigilance (Ridgway et al, 2006), and rats (Rattus norvegicus), which lack a NREM sleep rebound following 4 days of sleep deprivation (Rechtschaffen et al, 1999). Regardless of whether these exceptions are interpreted as evidence against a sleep homeostatic mechanism (Siegel, 2009) or as evidence of a poorly designed study (Cirelli and Tononi, 2008), in no case did the authors of those papers conclude that the animals do not sleep at all; the existence of 'sleep' as a state is not dependent on the demonstration of a particular kind of regulatory mechanism.…”

Section: Discussionmentioning

confidence: 99%

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Stephenson

Lewis

2011

Journal of Experimental Biology

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to sleep; resting wakefulness, paralysis, hibernation, torpor, akinesis, diapause, aestivation, anaesthesia and coma all share this characteristic. However, only in sleep and resting wakefulness is the suppression of motor output rapidly and spontaneously reversible. The second criterion, reversible suppression of sensory responsiveness, characterizes a quiescent state as sleep-like, and Accepted 15 November 2010 SUMMARY The objective of this study was to determine whether the great pond snail, Lymnaea stagnalis, expresses a sleep-like behavioural state. We found that snails spontaneously enter a relatively brief (22±1min) quiescent state characterized by postural relaxation of the foot, mantle and tentacles, and cessation of radula rasping. Quiescence was reversed ('aroused') by appetitive (sucrose solution) and aversive (tactile) stimuli. Responsiveness to both stimuli was significantly lower in quiescent snails than in active snails. However, tactile stimuli evoked a more sustained defensive response in quiescent snails. Quiescence bouts were consolidated into 'clusters' over an infradian timescale and were only weakly affected by time of day. Clusters contained 7±0.5 bouts, lasted 13±1h and were separated by long (37±4h) intervals of almost continuous activity. Analysis of Kaplan-Meier survival curves revealed that the quiescent bout duration was described by an exponential probability distribution (time constant 15±1min). Active bout duration was described by a bi-exponential probability distribution (time constants 62±4 and 592±48min). We found no evidence for a 'sleep rebound' mechanism and quiescence expression appeared to be regulated through stochastic processes causing state transitions to resemble a Markovian random walk. We conclude that Lymnaea is a potentially valuable model system for studies of cellular function in sleep.

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Section: Discussionmentioning

confidence: 99%

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Stephenson

Lewis

2011

Journal of Experimental Biology

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“…Auditory goal tone response time (AGTRT) did not slow between day one and day five whereas AGTRT was slower during night time (21:00-04:00 h) compared with daytime (09:00-16:00 h). However, the dolphins were able to maintain levels of vigilance as indicated by reliable goal tone detection even during night time periods of slowed AGTRT when the animals appeared to be resting or sleeping (Ridgway et al, 2006).…”

Section: Introductionmentioning

confidence: 94%

“…A previous study (Ridgway et al, 2006), reported for the first time that bottlenose dolphins (Tursiops truncatus) could maintain auditory vigilance for 120 continuous hours. These animals showed no evidence of sleep rebound or health effects of sleep deprivation as indicated by behavior, blood indices or marked sleep rebound during 24 h of continuous post-experiment observation.…”

Section: Introductionmentioning

confidence: 97%

Dolphins maintain cognitive performance during 72 to 120 hours of continuous auditory vigilance

Ridgway

Keogh

Carder

et al. 2009

Journal of Experimental Biology

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“…An increased number of glial cells in the cetacean brain, as seen herein when compared to artiodactyls, may result in an increased production of lactate. This extracellular lactate may be related to maintained arousal and attention during unihemispheric sleep (Ridgway et al, 2006(Ridgway et al, , 2009Branstetter et al, 2012), as extracellular lactate concentrations are higher during periods of wake (Pellerin and Magistretti, 1994). Furthermore lactate reduces extracellular pH levels and this is vital for arousal and attention, as orexinergic neurons are excited by a low pH (Williams et al, 2007;Parsons and Hirasawa, 2010).…”

Section: Orexinergic Bouton and Glial Cell Density Interaction In Thementioning

confidence: 99%

“…Additionally, it has been demonstrated that dolphins can continuously maintain vigilant behaviour for at least 15 days without any signs of sleep deprivation (Ridgway et al, 2006(Ridgway et al, , 2009Branstetter et al, 2012), an observation not made, but unlikely to be present in artiodactyls.…”

Section: Introductionmentioning

confidence: 99%

Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls

Dell

Spocter

Patzke

et al. 2015

Journal of Chemical Neuroanatomy

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Highlights• The orexinergic innervation of the cerebral cortex of Cetartiodactyla is described.• All species show a similar innervation pattern.• The density of innervation is far less in cetaceans than artiodactyls. 1 AbstractThe species of the cetacean and artiodactyl suborders, which make up the cetartiodactyl order, have very different arousal thresholds and sleep-wake systems.The aim of this study was to determine whether cetaceans or artiodactyls have differently organized orexinergic arousal systems by examining the density of orexinergic innervation to the cerebral cortex. This study provides a comparison of orexinergic bouton density in the cerebral cortex of twelve cetartiodactyl species by means of immunohistochemical staining and stereological analysis. It was observed that the morphology of the axonal projections of the orexinergic system to the cerebral cortex was similar across all species, as the presence, size and proportion of large and small orexinergic boutons were similar. Despite this, orexinergic bouton density was lower in the cerebral cortex of cetaceans compared to artiodactyls, even when corrected for brain mass, neuron density, glial density and glial: neuron ratio. Glial density was identified as the major determinant for the observed differences. It appears a synergy exists between the orexinergic neurons and their projections, glial cells, and the biochemical correlates of appetitive drive and arousal, but further studies need to be performed to understand the full extent of the orexinergic system and its role in sustained arousal.

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Dolphin continuous auditory vigilance for five days

Cited by 53 publications

References 32 publications

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus)

Dolphins maintain cognitive performance during 72 to 120 hours of continuous auditory vigilance

Orexinergic bouton density is lower in the cerebral cortex of cetaceans compared to artiodactyls

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