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8 - The evolution of wakefulness: From reptiles to mammals

Published online by Cambridge University Press:  10 March 2010

By
Ruben V. Rial ,
Mourad Akaârir ,
Antoni Gamundí ,
M. Cristina Nicolau  and
Susana Esteban
Edited by
Patrick McNamara ,
Robert A. Barton  and
Charles L. Nunn
Patrick McNamara
Affiliation:
Boston University
Robert A. Barton
Affiliation:
University of Durham
Charles L. Nunn
Affiliation:
Max Planck Institute for Evolutionary Anthropology
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Summary

Introduction

The evolution of sleep has been the subject of several studies and reviews (Allison & Cicchetti, 1976; Allison & Van Twyver, 1970; Hartse, 1994; Karmanova, 1982; Meddis, 1983; Monnier, 1980; Tauber, 1974). However, corresponding studies on the evolution of wakefulness have been fewer (Esteban, Nicolau, Gamundí, et al., 2005; Nicolau, Akaârir, Gamundí, et al., 2000), despite a number of reasons supporting the greater importance of waking in animal adaptation. First of all, waking and sleep are inseparable, an obvious assertion that, notwithstanding, has been ignored in most reviews (see, for instance, Zepelin, 1994; Zepelin & Rechtschaffen, 1974; Zepelin, Siegel, & Tobler, 2005). These reviews compute correlations between the main traits of sleep and ecological variables while forgetting that high correlations of a given trait with total sleep time also imply high correlations with waking time. The present review proposes a change of paradigm from sleep centeredness to waking centeredness.

Let us give an example of the paradigm change: there might be two possible viewpoints related to the high danger of a particular species' exposure within an environment, namely:

  1. Sleep is a dangerous state. Therefore natural selection must have reduced sleep in dangerous environments.

  2. Alertness is necessary to cope with danger. Therefore natural selection must have increased waking time in dangerous environments.

The difference between the two alternatives might seem subtle: but the former focuses on sleep as a key adaptive factor, while the latter is waking-centered.

Type
Chapter
Information
Evolution of Sleep
Phylogenetic and Functional Perspectives
 , pp. 172 - 196
Publisher: Cambridge University Press
Print publication year: 2009

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References

Aboitiz, F. (1992). The evolutionary origin of the mammalian cerebral cortex. Biological Research, 25, 41–49.Google ScholarPubMed
Aboitiz, F., Morales, D., & Montiel, J. (2003). The evolutionary origin of the mammalian isocortex: Towards an integrated developmental and functional approach. Behavioral Brain Sciences, 26, 535–586.CrossRefGoogle ScholarPubMed
Abrams, P. A. (2000). The evolution of predator-prey interactions: Theory and evidence. Annual Review of Ecology and Systematics, 31, 79–105.CrossRefGoogle Scholar
Allison, T., & Cicchetti, D. V. (1976). Sleep in mammals: Ecological and constitutional correlates. Science, 194, 732–734.CrossRefGoogle ScholarPubMed
Allison, T., & Van Twyver, H. (1970). The evolution of sleep. Natural History, 79, 57–65.Google Scholar
Amizca, F., & Steriade, M. (2002). The functional significance of K-complexes. Sleep Medicine Reviews, 6(2), 139–149.CrossRefGoogle Scholar
Aschoff, J. (1964). Survival value of diurnal rhythms. Symposiums of the Zoological Society of London, 13, 79–98.Google Scholar
Benington, J. H. (2000). Sleep homeostasis and the function of sleep. Sleep, 23(7), 959–966.CrossRefGoogle ScholarPubMed
Bowersox, S. S., Kaitin, K. I., & Dement, W. C. (1985). EEG spindle activity as a function of age: Relationships to sleep continuity. Brain Research, 334, 303–308.CrossRefGoogle Scholar
Braddick, J., Wattam-Bell, J., & Atkinson, J. (1986). Orientation specific cortical responses in early infancy. Nature, 320, 617–619.CrossRefGoogle ScholarPubMed
Bremer, F. (1935). Cerveau “isolé” et physiologie du sommeil [“Insulated” cerebrum and physiology of sleep]. Comptes Rendues Societé de Biologie (Paris), 118, 1235–1241.Google Scholar
Broughton, R. (1972). Phylogenetic evolution of sleep systems. In Chase, M. H. (Ed.), The sleeping brain: Proceedings of the symposia of the first international congress of the Association for the Physiological Study of Sleep (pp. 2–7). Los Angeles: Brain Research Institute.Google Scholar
Bruce, L. L., & Butler, A. B. (1984). Telencephalic connections in lizards. I. Projections to cortex. Journal of Comparative Neurology, 229, 585–561.CrossRefGoogle ScholarPubMed
Bullock, T. H. (2003). Have brain dynamics evolved? Should we look for unique dynamics in the sapient species?Neural Computation, 15, 2013–2027.CrossRefGoogle ScholarPubMed
Bullock, T. H., & Basar, E. (1988). Comparison of ongoing compound field potentials in the brain of invertebrates and vertebrates. Brain Research Reviews, 13, 57–75.CrossRefGoogle Scholar
Butler, A. B. (1974). The evolution of the dorsal pallium in the telencephalon of amniotes: Cladistic analysis and a new hypothesis. Brain Research Reviews, 19, 66–101.CrossRefGoogle Scholar
Butler, A. B., & Hodos, W. (2005). Comparative vertebrate neuroanatomy. Evolution and adaptation (4th ed.). New York: Wiley Liss.CrossRefGoogle Scholar
Campbell, C. B. G., & Hodos, W. (1970). The concept of homology and the evolution of the nervous system. Brain Behavior and Evolution, 3, 353–367.CrossRefGoogle ScholarPubMed
Carroll, R. I. (1988). Vertebrate paleontology and evolution. New York: Freeman Press.Google Scholar
Chalupa, L. M. (1991). Visual function of the pulvinar. In Leventhal, A. G. (Ed.), Vision and visual dysfunction: The neuronal basis of visual function (Vol. 4, pp. 140–159). London: MacMillan.Google Scholar
Church, M. W., Johnson, L. C., & Seales, D. M. (1978). Evoked K-complexes and cardiovascular responses to spindle-synchronous and spindle-asynchronous stimulus clicks during NREM sleep. Electroencephalography and Clinical Neurophysiology, 45, 443–453.CrossRefGoogle ScholarPubMed
Coenen, A. (1995). Neuronal activities underlying the electroencephalogram and evoked potentials in sleeping and waking: Implications for information processing. Neuroscience and Biobehavioral Process, 19, 447–463.CrossRefGoogle ScholarPubMed
Coenen, A., & Luijtelaar, E. L. J. M. (1985). Stress induced by three procedures of deprivation of paradoxical sleep. Physiology and Behavior, 35, 501–504.CrossRefGoogle ScholarPubMed
Crompton, A. W., Taylor, C., & Jagger, J. A. (1978) Evolution of homeothermy in mammals. Nature, 272, 333–336.CrossRefGoogle ScholarPubMed
Dawkins, R. (1986). The blind watchmaker. London: Penguin.Google Scholar
Iglesia, J. A. L., & López-García, C. (1997). Neuronal circuitry in the medial cerebral cortex of lizards. In Mira, J., Moreno-Díaz, R., & Cabestany, J. (Eds.), Proceedings of the international work-conference on artificial and natural neural networks: Biological and artificial computation: From neuroscience to technology (pp. 61–71). London: Springer-Verlag.Google Scholar
Vera, L., González, J., & Rial, R. V. (1994). Reptilian waking EEG: Slow waves, spindles and evoked potentials. Electroencephalographic and Clinical Neurophysiology, 90, 298–303.CrossRefGoogle ScholarPubMed
Dennett, D. C. (1995). Darwin's dangerous idea. London: Penguin.Google Scholar
Dringenberg, H. C., & Diavolitsis, P. (2002). Electroencephalographic activation by fluoxetine in rats: Role of 5-HT1A receptors and enhancement of concurrent acetylcholinesterase inhibitor treatment. Neuropharmacology, 42, 154–161.CrossRefGoogle Scholar
Dringenberg, H. C., & Vanderwolf, C. H. (1998). Involvement of direct and indirect pathways in electrocorticographic activation. Neuroscience and Biobehavioral Reviews, 22(2), 243–257.CrossRefGoogle ScholarPubMed
Edelmann, G. M., & Tononi, G. (2000). A universe of consciousness. New York: Basic Books.Google Scholar
Edelman, D. B., Baars, B. J., & Seth, A. K. (2005). Identifying hallmarks of consciousness in nonmammalian species. Consciousness and Cognition, 14, 169–187.CrossRefGoogle Scholar
Eichelbaum, H. (1998). Using olfaction to study memory. Annals of the New York Academy of Sciences, 855, 657–669.CrossRefGoogle Scholar
Esteban, S., Nicolau, M. C., Gamundí, A., Akaârir, M., & Rial, R. V. (2005) Animal sleep: Phylogenetic correlations. In Parmeggiani, P. L. & Velluti, R. (Eds.), The Physiologic nature of sleep (pp. 207–246). London: Imperial College Press.CrossRefGoogle Scholar
Feldman, S. M., & Waller, H. J. (1962). Dissociation of electrocortical activation and behavioural arousal. Nature, 196, 1320.CrossRefGoogle ScholarPubMed
Finlay, B. L., Hersman, M. N., & Darlington, R. B. (1998). Patterns of vertebrate neurogenesis and the paths of vertebrate evolution. Brain Behavior and Evolution, 52, 232–242.CrossRefGoogle ScholarPubMed
Garstang, W. (1922). The theory of recapitulation: A critical restatement of the biogenetic law. Zoological Journal of the Linnean Society London, 35, 81–101.CrossRefGoogle Scholar
Gaztelu, J. M., García-Austt, E., & Bullock, T. (1991). Electrocorticograms of hippocampal and dorsal cortex of two reptiles: Comparison with possible mammalian homologs. Brain Behavior and Evolution, 37, 144–160.CrossRefGoogle ScholarPubMed
Gómez, T., Bolaños, A., López, J. A., Nicolau, M. C., & Rial, R. (1990). A case report of spontaneous electrographic epilepsy in reptiles (Gallotia galloti). Comparative Biochemistry and Physiology, Series C, 97(2), 257–258.CrossRefGoogle Scholar
Gonzalez, A., & Ruschen, F. T. (1988). Connections of the basal ganglia in the lizard Gecko gecko. In Schwerdtfeger, W. K. & Smeets, W. J. A. (Eds.), The forebrain of reptiles (pp. 50–59). Basel: Karger.Google Scholar
González, J., & Rial, R. V. (1977). Electrofisiología de la corteza telencefálica de reptiles (Lacerta galloti): EEG y potenciales evocados [Electrophysiology of the telencephalic cortex of reptiles (Lacerta galloti): EEG and evoked potentials. Revista Española de Fisiología, 33, 239–248.Google Scholar
González, J., Vera, L. M., García-Cruz, C. M., & Rial, R. V. (1978). Efectos de la temperatura en el electroencefalograma y los potenciales evocados de los reptiles (Lacerta galloti) [Effects of the temperature in the electroencephalogram and the evoked potentials of the reptiles (Lacerta galloti)]. Revista Española de Fisiología, 34, 153–158.Google Scholar
Goren, C. C., Sarty, M., & Wu, P. Y. (1975). Visual following and pattern discrimination of face-like stimuli by newborn infants. Pediatrics, 56, 544–549.Google ScholarPubMed
Gould, S. J., & Levontin, R. C. (1979). The spandrels of San Marco and the Panglossian paradigm: A critique of the adaptationist programme. Proceedings of the Royal Society London, Series B, 205, 581–598.CrossRefGoogle Scholar
Guirado, S., Dávila, J. C., Real, M. A., & Medina, L. (2000). Light and electron microscopic evidence for projections from the thalamic nucleus rotundus to targets in the basal ganglia, the dorsal ventricular ridge, and the amygdaloid complex in a lizard. Journal of Comparative Neurology, 424(2), 216–232.3.0.CO;2-8>CrossRefGoogle Scholar
Habaguchi, T., Takakusaki, K., Sitoh, K., Sugimoto, J., & Sakamoto, T. (2002). Medullary reticulospinal tract mediating the generalized motor inhibition in cats: II. Functional organization within the medullary reticular formation with respect to postsynaptic inhibition of forelimb and hind-limb motoneurons. Neuroscience, 113(1), 65–77.CrossRefGoogle Scholar
Hartse, K. M. (1994). Sleep in insects and nonmammalian vertebrates. In Kryger, M. H., Roth, T., & Dement, W. C. (Eds.), Principles and practice of sleep medicine (pp. 95–104). London: Saunders.Google Scholar
Harvey, A. R., & Wortington, D. R. (1990). The projection from different visual cortical areas to the rat superior colliculus. Journal of Comparative Neurology, 298, 281–292.CrossRefGoogle ScholarPubMed
Hennig, W. (1966). Phylogenetic systematics. Urbana, IL: University of Illinois Press.Google Scholar
Hoogland, P. V., & Vermeulen Van Der Zee, E. (1989). Efferent connections of the dorsal cortex in the lizard Gecko gecko, studied with Phaseolus vulgaris leucoagglutinin. Journal of Comparative Neurology, 285, 289–303.CrossRefGoogle ScholarPubMed
Jane, J. A., Lewey, N., & Carlson, H. J. (1972). Tectal and cortical function in vision. Experimental Neurology, 35, 61–77.CrossRefGoogle ScholarPubMed
Jankel, W. R., & Niedermeyer, E. (1985). Sleep spindles. Journal of Clinical Neurophysiology, 37, 538–548.Google Scholar
Jerison, H. J. (1973). The evolution of the brain and intelligence. New York: Academic Press.Google Scholar
Jerison, H. J. (1990). Fossil evidence on the evolution of the neocortex. In Jones, E. G. & Peters, A. (Eds.), Cerebral cortex (pp. 285–309). New York: Plenum Press.Google Scholar
Johnson, M. H. (1990). Cortical maturation and the development of visual attention in early infancy. Journal of Cognitive Neuroscience, 2, 81–95.CrossRefGoogle ScholarPubMed
Karmanova, I. G. (1982). Evolution of sleep: Stages of the formation of the wakefulness-sleep cycle in vertebrates. Basel: Karger.Google Scholar
Kemp, T. S. (1982). Mammal-like reptiles and the origin of mammals. New York: Academic Press.Google Scholar
Kimura, M. (1983). The neutral theory of molecular evolution. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
Kupfermann, I., & Weiss, K. R. (1978). The command neuron concept. Behavioral Brain Sciences, 1, 3–39.CrossRefGoogle Scholar
Llinás, R., & Ribary, U. (1993). Coherent 40-Hz oscillation characterizes dream state in humans. Proceedings of the National Academy of Sciences of the United States of America, 90, 2078–2081.CrossRefGoogle ScholarPubMed
Lohman, A. H. M., & VanVoerden-Verkley, I. (1978). Ascending connections to the forebrain in the tegu lizard. Journal of Comparative Neurology, 182, 555–594.CrossRefGoogle ScholarPubMed
Lui, F., Giolli, R. A., Blanks, R. H., & Tom, E. M. (1994). Pattern of striate cortical projections to the pretectal complex in the guinea pig. Journal of Comparative Neurology, 344, 598–609.CrossRefGoogle ScholarPubMed
Lynch, G. (1986). Synapses, circuits, and the beginnings of memory. Cambridge, MA: MIT Press.Google Scholar
Malow, B. A., Carney, P. R., Kushwaha, R., & Bowes, R. J. (1999). Hippocampal sleep spindles revisited: Physiologic or epileptic activity?Clinical Neurophysiology, 110, 687–693.CrossRefGoogle ScholarPubMed
McCarley, R. W. (2007). Neurobiology of REM and NREM sleep. Sleep Medicine, 8, 302–330.CrossRefGoogle ScholarPubMed
Meddis, R. (1983). The evolution of sleep. In Mayes, A. (Ed.), Sleep mechanisms in humans and animals: An evolutionary perspective (pp. 57–106). London: Van Nostrand Reinhold.Google Scholar
Medina, L., Smeets, W. J. A. J., Hoogland, P. V., & Puelles, L. (1993). Distribution of choline acetyltransferase immunoreactivity in the brain of the lizard Gallotia galloti. Journal of Comparative Neurology, 331, 261–285.CrossRefGoogle ScholarPubMed
Monnier, M. (1980). Comparative electrophysiology of sleep in some vertebrates. Experientia, 36, 16–19.CrossRefGoogle ScholarPubMed
Montagnini, A., & Treves, A. (2003). The evolution of mammalian cortex from lamination to arealization. Brain Research Bulletin, 60, 387–393.CrossRefGoogle ScholarPubMed
Montero, V. (1993). Retinotopy of cortical connections between the striate cortex and extrastriate visual areas in the rat. Experimental Brain Research, 94, 1–15.CrossRefGoogle ScholarPubMed
Morton, J., & Johnson, M. H. (1991). CONSPEC and CONLEARN: A two-process theory of infant face recognition. Psychological Reviews, 98, 164–181.CrossRefGoogle ScholarPubMed
Muir, D. W., Clifton, R. K., & Clarkson, M. G. (1989). The development of a human auditory localization response: A U-shaped function. Canadian Journal of Psychology, 43, 199–216.CrossRefGoogle ScholarPubMed
Nicolau, M. C., Akaârir, M., Gamundí, A., González, J., & Rial, R. V. (2000). Why we sleep: The evolutionary pathway to the mammalian sleep. Progress in Neurobiology, 62, 379–406.CrossRefGoogle ScholarPubMed
Nobili, L., Ferrillo, F., Baglietto, M. G., Beelke, M., Carli, F., Negri, E., et al. (1999). Relationship of sleep interictal epileptiform discharges to sigma activity (12–16 Hz) in benign epilepsy of childhood with rolandic spikes. Clinical Neurophysiology, 110(1), 39–46.CrossRefGoogle ScholarPubMed
Parmeggiani, P. L. (2000). Physiological regulation in sleep. In Kryger, M. H., Roth, T. & Dement, W. C. (Eds.), Principles and practice of sleep medicine (pp. 169–178). Philadelphia: W. B. Saunders.Google Scholar
Pascalis, O., Haan, M., Nelson, C. A., & Schonen, S. (1998). Long-term recognition memory for faces assessed by visual paired comparison in 3- and 6-month old infants. Journal of Experimental Psychology: Learning, Memory, and Cognition, 24, 249–260.Google ScholarPubMed
Peterson, E. (1980). Behavioral studies of telencephalic function in reptiles. In Ebbeson, S. O. E. (Ed.), Comparative neurology of the telencephalon (pp. 343–388). New York: Plenum.CrossRefGoogle Scholar
Prechtl, J. C. (1994). Visual motion induces synchronous oscillations in turtle visual cortex. Proceedings of the National Academy of Sciences of the United States of America, 91, 12467–12471.CrossRefGoogle ScholarPubMed
Prechtl, J. C., Cohen, L. B., Pesaran, B., Mitra, P. P., & Kleinfeld, D. (1997). Visual stimuli induce waves of electrical activity in turtle cortex. Proceedings of the National Academy of Sciences of the United States of America, 94, 7621–7626.CrossRefGoogle ScholarPubMed
Prigogine, I., & Nicolis, G. (1977). Self-organization in non-equilibrium systems: From dissipative structures to order through fluctuations. New York: John Wiley & Sons.Google Scholar
Ramón Cajal, S. (1909). Histologie du Sytème Nerveux de l'homme et des vertébrésTome premier. Paris: A. Maloine. Reprint: 1952, Madrid: CSIC.Google Scholar
Rechtschaffen, A. (1971). The control of sleep. In Hunt, W. A. (Ed.), Human behaviour and its control (pp. 75–92). Cambridge, MA: Schenkman.Google Scholar
Rial, R. V., & González, J. (1978). Kindling effect in the reptilian brain: Motor and electrographic manifestations. Epilepsia, 19, 581–589.CrossRefGoogle ScholarPubMed
Rial, R. V., Nicolau, M. C., Gamundi, A., Akaârir, M., Aparicio, S., Garau, C., et al. (2007). The trivial function of sleep. Sleep Medicine Reviews, 11, 311–325.CrossRefGoogle ScholarPubMed
Rosa, M. G. P., & Kubitzer, L. A. (1999). The evolution of visual cortex: Where is V2?Trends in Neurosciences, 22, 242–248.CrossRefGoogle ScholarPubMed
Sagan, C. (1977). The dragons of Eden: Speculations on the evolution of human intelligence. New York: Ballantine Books.Google Scholar
Servit, Z., & Strejčkova, A. (1972). Thalamocortical relations and the genesis of epileptic electrographic phenomena in the forebrain of the turtle. Experimental Neurology, 35, 50–60.CrossRefGoogle ScholarPubMed
Servit, Z., Strejčkova, A., & Volanschi, D. (1971). Epileptic focus in the forebrain of the turtle (Testudo graeca). Triggering of focal discharges with different sensory stimuli. Physiologia Bohemoslovaca, 20, 221–228.Google ScholarPubMed
Sewards, T. V., & Sewards, M. A. (2002). Innate visual object recognition in vertebrates: Some proposed pathways and mechanisms. Comparative Biochemistry and Physiology, Series A, 132, 861–891.CrossRefGoogle ScholarPubMed
Siegel, J. M. (2001). The REM sleep-memory consolidation hypothesis. Science, 294, 1058–1063.CrossRefGoogle ScholarPubMed
Siegel, J. M., & McGinty, D. J. (1977). Pontine reticular neurons: Relationship of discharge to motor activity. Science, 196, 678–680.CrossRefGoogle ScholarPubMed
Sirota, A., Csicsvari, J., Buhl, D., & Buzsáki, G. (2003). Communication between neocortex and hippocampus during sleep in rodents. Proceedings of the National Academy of Sciences, 100(4), 2065–2069.CrossRefGoogle ScholarPubMed
Smeets, W. J. A. J., & Medina, L. (1995). The efferent connections of the nucleus accumbens in the lizard Gecko gecko. A combined tract-tracing transmitter-immunohistochemical study. Anatomical Embryology, 191, 73–81.Google ScholarPubMed
Sprague, J. M. (1966). Interactions of the cortex and superior colliculus in mediation of visually guided behaviour in the cat. Science, 153, 1544–1547.CrossRefGoogle Scholar
Steriade, M. (2000). Brain electrical activity and sensory processing during waking and sleeping states. In Kryger, M. H., Roth, T., & Dement, W. C. (Eds.), Principles and practice of sleep medicine (pp. 93–111). London: Saunders.Google Scholar
Steriade, M., & Amizca, F. (1998). Slow sleep oscillation, rhythmic K-complexes and their paroxismal developments. Journal of Sleep Research, 7(Suppl. 1), 30–35.CrossRefGoogle Scholar
Steriade, M., Curro-Dossi, R., & Nuñez, A. (1991). Network modulation of a slow intrinsic oscillation of cat thalamocortical neurons implicated in sleep delta waves: Cortical potentiation and brainstem cholinergic suppression. Journal of Neuroscience, 11, 200–217.CrossRefGoogle Scholar
Steriade, M., Oakson, G., & Ropert, N. (1982). Firing rates and patterns of midbrain reticular neurons during steady and transitional states of the sleep-waking cycle. Experimental Brain Research, 46, 37–51.CrossRefGoogle ScholarPubMed
Susic, V. (1972). Electrographic and behavioral correlations of the rest-activity cycle in the sea turtle, Caretta caretta L. (Chelonia). Journal of Experimental Marine Biology and Ecology, 10, 81–87.CrossRefGoogle Scholar
Takakusaki, K., Habaguchi, T., Ohtinata-Sugimoto, J., Saito, K., & Sakamoto, T. (2003). Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: A new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience, 119, 293–308.CrossRefGoogle ScholarPubMed
Tauber, E. S. (1974). Phylogeny of the sleep. Advances in Sleep Research, 1, 133–172.Google Scholar
Donkelaar, H. J. (1998). Reptiles. In Nieuvenhuis, R., Donkelaar, H. J., & Nicholson, C. (Eds.), The central nervous system of vertebrates (Vol. 2, pp. 1315–1524). Berlin: Springer.CrossRefGoogle Scholar
Donkelaar, H. J., & Boer-Van Huizen, R. (1981). Basal ganglia projections to the brain stem in the lizard Varanus exantematicus as demonstrated by retrograde transport of horseradish peroxidase. Neuroscience, 6, 1567–1590.CrossRefGoogle Scholar
Tumarkin, A. (1948). On the phylogeny of the mammalian auditory ossicles. Journal of Laryngology and Otology, 62, 687–690.CrossRefGoogle ScholarPubMed
Luijtelaar, E. L. J. M. (1997). Spike-wave discharges and sleep spindles in rats. Acta Neurobiologiae Experimentalis, 57, 113–121.Google ScholarPubMed
Vasilescu, E. (1970). Sleep and wakefulness in the tortoise (Emys orbicularis). Revue Roumaine de Biologie Serie de Zoologie, 15(3), 177–179.Google Scholar
Vertes, R. P. (2004). Memory consolidation in sleep: Dream or reality. Neuron, 1, 135–148.CrossRefGoogle Scholar
Vertes, R. P., & Eastman, K. E. (2000). The case against memory consolidation in REM sleep. Behavioral Brain Sciences, 23, 1057–1063.CrossRefGoogle ScholarPubMed
Voneida, T. J., & Sligar, C. M. (1979). Efferent projections of the dorsal ventricular ridge and the striatum in the tegu lizard, Tupinambis nigropuntatus. Journal of Comparative Neurology, 186, 43–64.CrossRefGoogle Scholar
Wallace, S. F., Rosenquist, A. C., & Sprague, J. M. (1990). Ibotenic acid lesions of the lateral substantia nigra restore visual orientation behavior in the hemianopic cat. Journal of Comparative Neurology, 296(2), 222–252.CrossRefGoogle ScholarPubMed
Williams, G. C. (1966). Adaptation and natural selection: A critique of some current evolutionary thought. Princeton, NJ: Princeton University Press.Google Scholar
Zepelin, H. (1994). Mammalian sleep. In Kryger, M. H., Roth, T., & Dement, W. C. (Eds.), Principles and practice of sleep medicine (pp. 69–80). Philadelphia: W. B. Saunders.Google Scholar
Zepelin, H., & Rechtschaffen, A. (1974). Mammalian sleep, longevity, and energy metabolism. Brain Behavior and Evolution, 10, 425–470.CrossRefGoogle ScholarPubMed
Zepelin, H., Siegel, J., & Tobler, I. (2005). Mammalian sleep. In Kryger, M. H., Roth, T., & Dement, W. C. (Eds.), Principles and practice of sleep medicine (pp. 91–100). Philadelphia: W. B. Saunders.CrossRefGoogle Scholar

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