Evolution of consciousness: Phylogeny, ontogeny, and emergence from general anesthesia

Are animals conscious? If so, when did consciousness evolve? We address these long-standing and essential questions using a modern neuroscientific approach that draws on diverse fields such as consciousness studies, evolutionary neurobiology, animal psychology, and anesthesiology. We propose that the stepwise emergence from general anesthesia can serve as a reproducible model to study the evolution of consciousness across various species and use current data from anesthesiology to shed light on the phylogeny of consciousness. Ultimately, we conclude that the neurobiological structure of the vertebrate central nervous system is evolutionarily ancient and highly conserved across species and that the basic neurophysiologic mechanisms supporting consciousness in humans are found at the earliest points of vertebrate brain evolution. Thus, in agreement with Darwin’s insight and the recent “Cambridge Declaration on Consciousness in Non-Human Animals,” a review of modern scientific data suggests that the differences between species in terms of the ability to experience the world is one of degree and not kind.

[1]  Laura D. Lewis,et al.  Rapid fragmentation of neuronal networks at the onset of propofol-induced unconsciousness , 2012, Proceedings of the National Academy of Sciences.

[2]  Hiroki R. Hayama,et al.  Event-related Functional Magnetic Resonance Imaging of a Low Dose of Dexmedetomidine that Impairs Long-term Memory , 2012, Anesthesiology.

[3]  Manuel S. Schröter,et al.  Spatiotemporal Reconfiguration of Large-Scale Brain Functional Networks during Propofol-Induced Loss of Consciousness , 2012, The Journal of Neuroscience.

[4]  Sten Grillner,et al.  Evolution of the basal ganglia: Dual‐output pathways conserved throughout vertebrate phylogeny , 2012, The Journal of comparative neurology.

[5]  H. Blumenfeld Impaired consciousness in epilepsy , 2012, The Lancet Neurology.

[6]  Cornelis J. Stam,et al.  Go with the flow: Use of a directed phase lag index (dPLI) to characterize patterns of phase relations in a large-scale model of brain dynamics , 2012, NeuroImage.

[7]  W. Singer,et al.  Thalamic Coordination of Cortical Communication , 2012, Neuron.

[8]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[9]  M. Boly,et al.  Neural correlates of consciousness during general anesthesia using functional magnetic resonance imaging (fMRI). , 2012, Archives italiennes de biologie.

[10]  Raymond Noack Solving the “human problem”: The frontal feedback model , 2012, Consciousness and Cognition.

[11]  C. Stam,et al.  The organization of physiological brain networks , 2012, Clinical Neurophysiology.

[12]  Hiroki R. Hayama,et al.  Returning from Oblivion: Imaging the Neural Core of Consciousness , 2012, The Journal of Neuroscience.

[13]  W. Singer,et al.  Neuroscience and Biobehavioral Reviews Distilling the Neural Correlates of Consciousness , 2022 .

[14]  Po-Jang Hsieh,et al.  The ‘correlates’ in neural correlates of consciousness , 2012, Neuroscience & Biobehavioral Reviews.

[15]  Hal Blumenfeld,et al.  Epilepsy and the consciousness system: transient vegetative state? , 2011, Neurologic clinics.

[16]  UnCheol Lee,et al.  Preferential Inhibition of Frontal-to-Parietal Feedback Connectivity Is a Neurophysiologic Correlate of General Anesthesia in Surgical Patients , 2011, PloS one.

[17]  J. Panksepp Cross-Species Affective Neuroscience Decoding of the Primal Affective Experiences of Humans and Related Animals , 2011, PloS one.

[18]  James R. Anderson,et al.  Do rhesus monkeys recognize themselves in mirrors? , 2011, American journal of primatology.

[19]  E. Brown,et al.  General anesthesia and altered states of arousal: a systems neuroscience analysis. , 2011, Annual review of neuroscience.

[20]  L. M. Ward,et al.  The thalamic dynamic core theory of conscious experience , 2011, Consciousness and Cognition.

[21]  A. Morin,et al.  Self-recognition, theory-of-mind, and self-awareness: What side are you on? , 2011, Laterality.

[22]  UnCheol Lee,et al.  Dissociable Network Properties of Anesthetic State Transitions , 2011, Anesthesiology.

[23]  A Dagher,et al.  Critical involvement of the thalamus and precuneus during restoration of consciousness with physostigmine in humans during propofol anaesthesia: a positron emission tomography study. , 2011, British journal of anaesthesia.

[24]  Arend Hintze,et al.  Integrated Information Increases with Fitness in the Evolution of Animats , 2011, PLoS Comput. Biol..

[25]  E. Brown,et al.  General anesthesia, sleep, and coma. , 2010, The New England journal of medicine.

[26]  Abigail Z. Rajala,et al.  Rhesus Monkeys (Macaca mulatta) Do Recognize Themselves in the Mirror: Implications for the Evolution of Self-Recognition , 2010, PloS one.

[27]  Q. C. Meng,et al.  A Conserved Behavioral State Barrier Impedes Transitions between Anesthetic-Induced Unconsciousness and Wakefulness: Evidence for Neural Inertia , 2010, PloS one.

[28]  Byoung-Kyong Min,et al.  A thalamic reticular networking model of consciousness , 2010, Theoretical Biology and Medical Modelling.

[29]  UnCheol Lee,et al.  The directionality and functional organization of frontoparietal connectivity during consciousness and anesthesia in humans , 2009, Consciousness and Cognition.

[30]  J. Hobson,et al.  REM sleep and dreaming: towards a theory of protoconsciousness , 2009, Nature Reviews Neuroscience.

[31]  G. F. Egan,et al.  The role of primordial emotions in the evolutionary origin of consciousness , 2009, Consciousness and Cognition.

[32]  J. Hohwy The neural correlates of consciousness: New experimental approaches needed? , 2009, Consciousness and Cognition.

[33]  A. Nieder Prefrontal cortex and the evolution of symbolic reference , 2009, Current Opinion in Neurobiology.

[34]  UnCheol Lee,et al.  Propofol induction reduces the capacity for neural information integration: Implications for the mechanism of consciousness and general anesthesia , 2008, Consciousness and Cognition.

[35]  G. Tononi,et al.  Consciousness and Anesthesia , 2008, Science.

[36]  O. Güntürkün,et al.  Mirror-Induced Behavior in the Magpie (Pica pica): Evidence of Self-Recognition , 2008, PLoS biology.

[37]  Miriam K. Konkel,et al.  Genome analysis of the platypus reveals unique signatures of evolution , 2008, Nature.

[38]  N. Franks General anaesthesia: from molecular targets to neuronal pathways of sleep and arousal , 2008, Nature Reviews Neuroscience.

[39]  A. Butler Evolution of brains, cognition, and consciousness , 2008, Brain Research Bulletin.

[40]  J. Capizzi Consciousness in Human and Nonhuman Animals , 2008 .

[41]  Johannes Jacobus Fahrenfort,et al.  The spatiotemporal profile of cortical processing leading up to visual perception. , 2008, Journal of vision.

[42]  Christof Koch,et al.  The Neural Correlates of Consciousness , 2007, Scholarpedia.

[43]  N. Block Consciousness, accessibility, and the mesh between psychology and neuroscience , 2007, Behavioral and Brain Sciences.

[44]  S. Dehaene,et al.  Subliminal words durably affect neuronal activity , 2007, Neuroreport.

[45]  Olivier Gascuel,et al.  Genomics, biogeography, and the diversification of placental mammals , 2007, Proceedings of the National Academy of Sciences.

[46]  M. Boly,et al.  Baseline brain activity fluctuations predict somatosensory perception in humans , 2007, Proceedings of the National Academy of Sciences.

[47]  B. Merker Consciousness without a cerebral cortex: A challenge for neuroscience and medicine , 2007, Behavioral and Brain Sciences.

[48]  Diana Reiss,et al.  Self-recognition in an Asian elephant , 2006, Proceedings of the National Academy of Sciences.

[49]  V. Lamme Towards a true neural stance on consciousness , 2006, Trends in Cognitive Sciences.

[50]  R. Cotterill,et al.  Mammalian and Avian Neuroanatomy and the Question of Consciousness in Birds , 2006, The Biological Bulletin.

[51]  B. Waterhouse,et al.  Locus Ceruleus Regulates Sensory Encoding by Neurons and Networks in Waking Animals , 2006, The Journal of Neuroscience.

[52]  S. Dehaene,et al.  Nonconscious semantic processing of emotional words modulates conscious access. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[53]  N. Emery Cognitive ornithology: the evolution of avian intelligence , 2006, Philosophical Transactions of the Royal Society B: Biological Sciences.

[54]  Nicola S. Clayton,et al.  Evolution of the avian brain and intelligence , 2005, Current Biology.

[55]  Steven Laureys The neural correlate of (un)awareness: lessons from the vegetative state , 2005, Trends in Cognitive Sciences.

[56]  Helen A. Baghdoyan,et al.  Sleep, Anesthesiology, and the Neurobiology of Arousal State Control , 2005, Anesthesiology.

[57]  A. Revonsuo Inner Presence: Consciousness as a Biological Phenomenon , 2005 .

[58]  Anthony G. Hudetz,et al.  Volatile anesthetics disrupt frontal-posterior recurrent information transfer at gamma frequencies in rat , 2005, Neuroscience Letters.

[59]  A. Butler,et al.  Evolution of the neural basis of consciousness: a bird-mammal comparison. , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[60]  B. Baars Subjective experience is probably not limited to humans: The evidence from neurobiology and behavior , 2005, Consciousness and Cognition.

[61]  James L McGaugh,et al.  Emotional arousal and enhanced amygdala activity: new evidence for the old perseveration-consolidation hypothesis. , 2005, Learning & memory.

[62]  B. Baars,et al.  Criteria for consciousness in humans and other mammals , 2005, Consciousness and Cognition.

[63]  Gerald E. Hough,et al.  Avian brains and a new understanding of vertebrate brain evolution , 2005, Nature Reviews Neuroscience.

[64]  Nicola S. Clayton,et al.  The Mentality of Crows: Convergent Evolution of Intelligence in Corvids and Apes , 2004, Science.

[65]  G. Tononi An information integration theory of consciousness , 2004, BMC Neuroscience.

[66]  Steven Laureys,et al.  Brain function in coma, vegetative state, and related disorders , 2004, The Lancet Neurology.

[67]  Jennifer T Coull,et al.  Attentional effects of noradrenaline vary with arousal level: selective activation of thalamic pulvinar in humans , 2004, NeuroImage.

[68]  G. Gallup,et al.  Let ’ s Face It A review of The Face in the Mirror : The Search for the Origins of Consciousness , 2003 .

[69]  J. Changeux,et al.  A neuronal network model linking subjective reports and objective physiological data during conscious perception , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Antonio Damasio,et al.  Mental self: The person within , 2003, Nature.

[71]  Larry Cahill,et al.  Epinephrine enhancement of human memory consolidation: Interaction with arousal at encoding , 2003, Neurobiology of Learning and Memory.

[72]  C. Koch,et al.  A framework for consciousness , 2003, Nature Neuroscience.

[73]  Peter Herscovitch,et al.  The process of awakening: a PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness. , 2002, Brain : a journal of neurology.

[74]  M. Witter,et al.  The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness , 2002, Brain Research Reviews.

[75]  H. Damasio,et al.  Humans and great apes share a large frontal cortex , 2002, Nature Neuroscience.

[76]  D. Long I of the Vortex: From Neurons to Self , 2002 .

[77]  N. Emery,et al.  Effects of experience and social context on prospective caching strategies by scrub jays , 2001, Nature.

[78]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[79]  D. Reiss,et al.  Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[80]  R. Cotterill Cooperation of the basal ganglia, cerebellum, sensory cerebrum and hippocampus: possible implications for cognition, consciousness, intelligence and creativity , 2001, Progress in Neurobiology.

[81]  F. Delfour,et al.  Mirror image processing in three marine mammal species: killer whales (Orcinus orca), false killer whales (Pseudorca crassidens) and California sea lions (Zalophus californianus) , 2001, Behavioural Processes.

[82]  M Liotti,et al.  Brain responses associated with consciousness of breathlessness (air hunger). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[83]  F. Plum,et al.  The Role of Arousal and “Gating” Systems in the Neurology of Impaired Consciousness , 2000, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[84]  Anil K. Seth,et al.  Consciousness and Complexity , 2022 .

[85]  G K Aguirre,et al.  Neural components of topographical representation. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[86]  Richard T. Marrocco,et al.  Arousal systems , 1994, Current Opinion in Neurobiology.

[87]  R. Llinás,et al.  Coherent 40-Hz oscillation characterizes dream state in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[88]  A. Reeves,et al.  The Triune Brain in Evolution: Role in Paleocerebml Functions , 1992 .

[89]  Gordon G. Gallup,et al.  Do minds exist in species other than our own? , 1985, Neuroscience & Biobehavioral Reviews.

[90]  Jason C. Birnholz,et al.  The development of human fetal eye movement patterns. , 1981, Science.

[91]  G. Gallup Chimpanzees: Self-Recognition , 1970, Science.

[92]  G Tononi,et al.  Integrated information theory of consciousness: an updated account. , 2012, Archives italiennes de biologie.

[93]  B. G. Goodrich We Do, Therefore We Think: Time, Motility, and Consciousness , 2010, Reviews in the neurosciences.

[94]  J. Jing,et al.  Evolving Concepts of Arousal: Insights from Simple Model Systems , 2009, Reviews in the neurosciences.

[95]  R. Brusseau Developmental Perspectives: is the Fetus Conscious? , 2008, International anesthesiology clinics.

[96]  D. Denton The Primordial Emotions: The Dawning of Consciousness , 2006 .

[97]  G. Striedter Principles of brain evolution. , 2005 .

[98]  T. Paus Functional anatomy of arousal and attention systems in the human brain. , 2000, Progress in brain research.

[99]  F. Crick The Astonishing Hypothesis , 1994 .

[100]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[101]  B. Amsterdam,et al.  Mirror self-image reactions before age two. , 1972, Developmental psychobiology.

[102]  G. G. Gallop Chimpanzees: self-recognition. , 1970, Science.

[103]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[104]  C. Darwin,et al.  The Expression of the Emotions in Man and Animals , 1872 .