Characterization of sleep in Aplysia californica.

STUDY OBJECTIVE To characterize sleep in the marine mollusk, Aplysia californica. DESIGN Animal behavior and activity were assessed using video recordings to measure activity, resting posture, resting place preference, and behavior after rest deprivation. Latencies for behavioral responses were measured for appetitive and aversive stimuli for animals in the wake and rest states. SETTING Circadian research laboratory for Aplysia. PATIENTS OR PARTICIPANTS A. californica from the Pacific Ocean. INTERVENTIONS N/A. MEASUREMENTS AND RESULTS Aplysia rest almost exclusively during the night in a semi-contracted body position with preferential resting locations in the upper corners of their tank. Resting animals demonstrate longer latencies in head orientation and biting in response to a seaweed stimulus and less frequent escape response steps following an aversive salt stimulus applied to the tail compared to awake animals at the same time point. Aplysia exhibit rebound rest the day following rest deprivation during the night, but not after similar handling stimulation during the day. CONCLUSIONS Resting behavior in Aplysia fulfills all invertebrate characteristics of sleep including: (1) a specific sleep body posture, (2) preferred resting location, (3) reversible behavioral quiescence, (4) elevated arousal thresholds for sensory stimuli during sleep, and (5) compensatory sleep rebound after sleep deprivation.

[1]  W. O. Haufe.  Ethological and Statistical Aspects of a Quantal Response in Mosquitoes To Environmental Stimuli 1) , 1963 .

[2]  I. Kupfermann.  A circadian locomotor rhythm in Aplysia Californica , 1968 .

[3]  F. Strumwasser.  THE CELLULAR BASIS OF BEHAVIOR IN APLYSIA , 1972 .

[4]  Lee Rm,et al.  Feeding behavior in Aplysia californica: role of chemical and tactile stimuli. , 1973 .

[5]  F. Strumwasser.  Seventeenth Bowditch lecture. Neural and humoral factors in the temporal organization of behavior. , 1973, The Physiologist.

[6]  R. M. Lee,et al.  Feeding behavior in Aplysia californica: role of chemical and tactile stimuli. , 1973, Journal of comparative and physiological psychology.

[7]  W. F. Flanigan,et al.  Sleep and wakefulness in iguanid lizards, Ctenosaura pectinata and Iguana iguana. , 1973, Brain, behavior and evolution.

[8]  J. F. Flanigan.  Sleep and Wakefulness in Iguanid Lizards, Ctenosaura pectinata and Iguana iguana; pp. 401–416 , 1973 .

[9]  I. Kupfermann.  Feeding behavior in Aplysia: a simple system for the study of motivation. , 1974, Behavioral biology.

[10]  R. M. Lee,et al.  Behavioral states and feeding in the gastropod Pleurobranchaea. , 1976, Behavioral biology.

[11]  B. Jahan-Parwar,et al.  Neural control of locomotion in Aplysia: role of the central ganglia. , 1979, Behavioral and neural biology.

[12]  E. Kandel,et al.  Motorneuronal control of locomotion in Aplysia , 1979, Brain Research.

[13]  A. Borbély.  A two process model of sleep regulation. , 1982, Human neurobiology.

[14]  E. Kandel,et al.  Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. , 1983, Journal of neurophysiology.

[15]  Walter Kaiser,et al.  Neuronal correlates of sleep, wakefulness and arousal in a diurnal insect , 1983, Nature.

[16]  Irene Tobler,et al.  Effect of forced locomotion on the rest-activity cycle of the cockroach , 1983, Behavioural Brain Research.

[17]  Abraham J Susswein,et al.  Activity patterns and time budgeting of Aplysia fasciata under field and laboratory conditions. , 1983, Behavioral and neural biology.

[18]  Scott S. Campbell,et al.  Animal sleep: A review of sleep duration across phylogeny , 1984, Neuroscience & Biobehavioral Reviews.

[19]  J. Leonard,et al.  The Behavior of Aplysia Californica Cooper (Gastropoda; Opisthobranchia): I. Ethogram , 1986 .

[20]  S. Fredman,et al.  Recovery of escape locomotion following a CNS lesion in Aplysia. , 1988, Behavioral and neural biology.

[21]  Daily variation of multiple behaviors in Aplysia fasciata: integration of feeding, reproduction, and locomotion. , 1991, Behavioral and neural biology.

[22]  I. Tobler,et al.  24‐h variation of vigilance in the cockroach Blaberus giganteus , 1992, Journal of sleep research.

[23]  J. Byrne,et al.  Identification and characterization of a multifunction neuron contributing to defensive arousal in Aplysia. , 1993, Journal of neurophysiology.

[24]  M. Miller,et al.  Behavior Patterns of the Aplysiid Gastropod Bursatella leachii in Its Natural Habitat and in the Laboratory , 1995, Neurobiology of Learning and Memory.

[25]  W. Kaiser.  Rest at night in some solitary bees - a comparison with the sleep-like state of honey bees , 1995 .

[26]  Irene Tobler,et al.  Is sleep fundamentally different between mammalian species? , 1995, Behavioural Brain Research.

[27]  T. Roth,et al.  Sleep disturbance and psychiatric disorders: A longitudinal epidemiological study of young Adults , 1996, Biological Psychiatry.

[28]  Paul E. Hardin,et al.  Circadian rhythms in olfactory responses of Drosophila melanogaster , 1999, Nature.

[29]  J. Byrne,et al.  Levels of Serotonin in the Hemolymph of AplysiaAre Modulated by Light/Dark Cycles and Sensitization Training , 1999, The Journal of Neuroscience.

[30]  P. Achermann,et al.  Sleep Homeostasis and Models of Sleep Regulation , 1999 .

[31]  A. Pack,et al.  The need for a simple animal model to understand sleep , 2000, Progress in Neurobiology.

[32]  Allan I Pack,et al.  Rest in Drosophila Is a Sleep-like State , 2000, Neuron.

[33]  G. Tononi,et al.  Correlates of sleep and waking in Drosophila melanogaster. , 2000, Science.

[34]  E. Kandel.  The Molecular Biology of Memory Storage: A Dialogue Between Genes and Synapses , 2001, Science.

[35]  I. Zhdanova,et al.  Melatonin promotes sleep-like state in zebrafish 1 1 Published on the World Wide Web on 6 April 2001. , 2001, Brain Research.

[36]  Russell J. Schmitt,et al.  Competition for shelter space causes density-dependent predation mortality in damselfishes , 2002 .

[37]  P. Achermann,et al.  Mathematical models of sleep regulation. , 2003, Frontiers in bioscience : a journal and virtual library.

[38]  A. Eskin,et al.  Circadian modulation of long-term sensitization in Aplysia , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  T. Page,et al.  Circadian rhythm in olfactory response in the antennae controlled by the optic lobe in the cockroach. , 2003, Journal of insect physiology.

[40]  Katsumi Yoshida,et al.  Persistent Insomnia is a Predictor of Hypertension in Japanese Male Workers , 2003, Journal of occupational health.

[41]  J. Jacklet.  Circadian locomotor activity inAplysia , 1972, Journal of comparative physiology.

[42]  T. Bullock,et al.  Slow wave sleep in crayfish. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[43]  R. Holzman,et al.  Aeration of corals by sleep‐swimming fish , 2004 .

[44]  Giulio Tononi,et al.  Sleep homeostasis in Drosophila melanogaster. , 2004, Sleep.

[45]  Irene Tobler,et al.  Rest in the scorpion — a sleep-like state? , 1988, Journal of Comparative Physiology A.

[46]  W. Kaiser.  Busy bees need rest, too , 1988, Journal of Comparative Physiology A.

[47]  M. T. Erickson,et al.  Directional control and the functional organization of defensive responses inAplysia , 1986, Journal of Comparative Physiology A.

[48]  W. Kaiser,et al.  Sleep deprivation in honey bees 1 , 2004, Journal of sleep research.

[49]  Esteban O. Mazzoni,et al.  Circadian Pacemaker Neurons Transmit and Modulate Visual Information to Control a Rapid Behavioral Response , 2005, Neuron.

[50]  G. Tononi,et al.  Breakdown of Cortical Effective Connectivity During Sleep , 2005, Science.

[51]  E. Herzog,et al.  A Circadian Clock in the Olfactory Bulb Controls Olfactory Responsivity , 2006, The Journal of Neuroscience.

[52]  John A. Lesku,et al.  The Evolution of Sleep: A Phylogenetic Approach , 2006 .

[53]  E. Brown,et al.  Brain and behavioural evidence for rest-activity cycles in Octopus vulgaris , 2006, Behavioural Brain Research.

[54]  B. Feige,et al.  Increased nocturnal interleukin-6 excretion in patients with primary insomnia: A pilot study , 2006, Brain, Behavior, and Immunity.

[55]  Giulio Tononi,et al.  Exploratory behavior, cortical BDNF expression, and sleep homeostasis. , 2007, Sleep.

[56]  Emmanuel Mignot,et al.  Characterization of Sleep in Zebrafish and Insomnia in Hypocretin Receptor Mutants , 2007, PLoS biology.

[57]  Arnstein Mykletun,et al.  Chronic insomnia as a risk factor for developing anxiety and depression. , 2007, Sleep.

[58]  David M. Raizen,et al.  Conservation of sleep: insights from non-mammalian model systems , 2008, Trends in Neurosciences.

[59]  G. Bloch,et al.  Differences in the sleep architecture of forager and young honeybees (Apis mellifera) , 2008, Journal of Experimental Biology.

[60]  E. Kandel,et al.  Transcriptional regulation of long-term memory in the marine snail Aplysia , 2008, Molecular Brain.

[61]  David M. Raizen,et al.  Lethargus is a Caenorhabditis elegans sleep-like state , 2008, Nature.

[62]  G. Tononi,et al.  Is Sleep Essential? , 2008, PLoS biology.

[63]  Thomas D. Seeley,et al.  Caste-dependent sleep of worker honey bees , 2008, Journal of Experimental Biology.

[64]  M. Peterson,et al.  Insomnia and depression. , 2008, Sleep medicine.

[65]  E. Walters,et al.  Molluscan Memory of Injury: Evolutionary Insights into Chronic Pain and Neurological Disorders , 2009, Brain, Behavior and Evolution.

[66]  Giulio Tononi,et al.  Breakdown of effective connectivity during slow wave sleep: investigating the mechanism underlying a cortical gate using large-scale modeling. , 2009, Journal of neurophysiology.

[67]  Sleep and its possible role in learning: a phylogenetic view. , 2009 .

[68]  Sleep and its possible role in learning: a phylogenetic view. , 2009, Frontiers in bioscience.

[69]  R. Menzel,et al.  Sleep deprivation affects extinction but not acquisition memory in honeybees. , 2009, Learning & memory.

[70]  D. Dinges,et al.  Neurocognitive consequences of sleep deprivation. , 2005, Seminars in neurology.

[71]  Duanping Liao,et al.  Insomnia with objective short sleep duration is associated with a high risk for hypertension. , 2009, Sleep.

[72]  G. Tononi,et al.  Effects of skilled training on sleep slow wave activity and cortical gene expression in the rat. , 2009, Sleep.

[73]  Rachel Leproult,et al.  Role of sleep and sleep loss in hormonal release and metabolism. , 2010, Endocrine development.

[74]  F. Ramón,et al.  Slow waves during sleep in crayfish. Origin and spread , 2010, Journal of Experimental Biology.

[75]  D. Goldstein,et al.  Lobster Attack Induces Sensitization in the Sea Hare, Aplysia californica , 2010, The Journal of Neuroscience.

[76]  Sleep homeostasis: Progress at a snail's pace. , 2011, Communicative & integrative biology.

[77]  Irene Tobler,et al.  Chapter 9 – Phylogeny of Sleep Regulation , 2011 .

[78]  K. Hartse.  The phylogeny of sleep. , 2011, Handbook of clinical neurology.

[79]  Richard Stephenson,et al.  Behavioural evidence for a sleep-like quiescent state in a pulmonate mollusc, Lymnaea stagnalis (Linnaeus) , 2011, Journal of Experimental Biology.

[80]  T. Murase,et al.  Association of short sleep duration with obesity, diabetes, fatty liver and behavioral factors in Japanese men. , 2011, Internal medicine.

[81]  T. Carew,et al.  The tail-elicited tail withdrawal reflex of Aplysia is mediated centrally at tail sensory-motor synapses and exhibits sensitization across multiple temporal domains. , 2011, Learning & memory.

[82]  A. Borbély,et al.  Manifestations and functional implications of sleep homeostasis. , 2011, Handbook of clinical neurology.

[83]  Sara J. Aton,et al.  A Preliminary Analysis of Sleep-Like States in the Cuttlefish Sepia officinalis , 2012, PloS one.

[84]  P. Gehrman,et al.  Sleep disturbance is associated with cardiovascular and metabolic disorders , 2012, Journal of sleep research.

[85]  T. Porkka-Heiskanen,et al.  Sleep homeostasis , 2013, Current Opinion in Neurobiology.

[86]  B. van Swinderen,et al.  A Dynamic Deep Sleep Stage in Drosophila , 2013, The Journal of Neuroscience.

[87]  M. Michel,et al.  Protein Phosphatase-Dependent Circadian Regulation of Intermediate-Term Associative Memory , 2013, The Journal of Neuroscience.