Criteria for consciousness in humans and other mammals

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Abstract

The standard behavioral index for human consciousness is the ability to report events with accuracy. While this method is routinely used for scientific and medical applications in humans, it is not easy to generalize to other species. Brain evidence may lend itself more easily to comparative testing. Human consciousness involves widespread, relatively fast low-amplitude interactions in the thalamocortical core of the brain, driven by current tasks and conditions. These features have also been found in other mammals, which suggests that consciousness is a major biological adaptation in mammals. We suggest more than a dozen additional properties of human consciousness that may be used to test comparative predictions. Such homologies are necessarily more remote in non-mammals, which do not share the thalamocortical complex. However, as we learn more we may be able to make “deeper” predictions that apply to some birds, reptiles, large-brained invertebrates, and perhaps other species.

Section snippets

The limits of behavioral criteria

“Accurate report” (AR) is the standard behavioral index for consciousness in humans. Accurate report is extremely useful and sensitive in people with intact brains. For example, we can report the light of a star on a dark night, involving a flow of single photons to a single retinal receptor. This conscious event corresponds to the lower limit of physical energy. Similarly subtle percepts are reportable in audition and touch. AR can thus be highly sensitive and accurate.

Accurate report in

Consciousness and the brain

Physiologically, three basic facts stand out about consciousness.

Putting it all together

How, in practice, can these properties be used to test comparative predictions about consciousness? Considering this question raises the issue that the foregoing properties vary considerably in their testability. Those that have to do with structural homologies of neuroanatomy are relatively easy to test; it is not difficult to identify a thalamocortical complex in a monkey or in a dog (criterion #2).

Conclusions

Contrary to widespread belief, the question of animal consciousness is not unapproachable. Human consciousness depends on well-established properties of the thalamocortical complex, a structure that is shared with other mammals. While a great deal remains to be discovered, there are at least 17 properties that can also be tested, with varying degrees of precision, in other species.

Acknowledgments

This work was supported by The Neuroscience Institute and the Neuroscience Research Foundation, which are gratefully acknowledged. We thank Drs. Gerald M. Edelman and Bjorn Merker for constructive comments.

References (107)

  • C.M. Gray

    The temporal correlation hypothesis of visual feature integration: Still alive and well

    Neuron

    (1999)
  • A.M. Graybiel

    Building action repertoires: Memory and learning functions of the basal ganglia

    Current Opinion in Neurobiology

    (1995)
  • N.K. Logothetis

    MR imaging in the non-human primate: Studies of function and of dynamic connectivity

    Current Opinion in Neurobiology

    (2003)
  • K. Louie et al.

    Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep

    Neuron

    (2001)
  • B. Mangan

    Taking phenomenology seriously: The fringe and its implications for cognitive research

    Consciousness and Cognition

    (1993)
  • A. Maril et al.

    On the tip of the tongue: An event-related fMRI study of semantic retrieval failure and cognitive conflict

    Neuron

    (2001)
  • P.M. Merikle et al.

    Perception without awareness: Perspectives from cognitive psychology

    Cognition

    (2001)
  • S.G. Rayport et al.

    Development of plastic mechanisms related to learning at identified chemical synaptic connections in Aplysia

    Neuroscience

    (1986)
  • M.N. Shadlen et al.

    Synchrony unbound: A critical evaluation of the temporal binding hypothesis

    Neuron

    (1999)
  • J.M. Siegel et al.

    Sleep in the platypus

    Neuroscience

    (1999)
  • W. Singer

    Neuronal synchrony: A versatile code for the definition of relations?

    Neuron

    (1999)
  • K.M. Stephan et al.

    Conscious and subconscious sensorimotor synchronization–prefrontal cortex and the influence of awareness

    Neuroimage

    (2002)
  • G. Tononi et al.

    Complexity and coherency: Integrating information in the brain

    Trends in Cognitive Sciences

    (1998)
  • G. Tononi et al.

    Functional clustering: Identifying strongly interactive brain regions in neuroimaging data

    Neuroimage

    (1998)
  • B.J. Baars

    A cognitive theory of consciousness

    (1988)
  • B.J. Baars

    How brain reveals mind: Neuroimaging supports the fundamental role of conscious experience

    Journal of Consciousness Studies

    (2003)
  • H. Berger

    Ueber das Elektroenkephalogramm des Menschen

    Archiv fuer Psyhiatrie und Nervenkrankheiten, Berlin

    (1929)
  • N. Block et al.

    Dualism, conceptual analysis, and the explanatory gap

    Philosophical Review

    (1999)
  • K.S. Bowers et al.

    Intuition in the context of discovery

    Cognitive Psychology

    (1990)
  • Brentano, F. (1924–28). Psychologie vom empirischen standpunkt. Leipzig:...
  • A.A. Brewer et al.

    Visual areas in macaque cortex measured using functional magnetic resonance imaging

    Journal of Neuroscience

    (2002)
  • D.J. Chalmers

    The puzzle of conscious experience

    Scientific American

    (1995)
  • N. Cowan

    The magical number 4 in short-term memory: A reconsideration of mental storage capacity

    Behavioral and Brain Sciences

    (2001)
  • A. Cowey et al.

    Blindsight in monkeys

    Nature

    (1995)
  • F. Crick

    Function of the thalamic reticular complex: The searchlight hypothesis

    Proceedings of the National Academy of Sciences of the United States of America

    (1984)
  • F. Crick et al.

    Some reflections on visual awareness

    Cold Spring Harbour Symposium Quantitative Biology

    (1990)
  • S. Dehaene et al.

    Cerebral mechanisms of word masking and unconscious repetition priming

    Nature Neuroscience

    (2001)
  • D. Denton et al.

    Neuroimaging of genesis and satiation of thirst and an interoceptor-driven theory of origins of primary consciousness

    Proceedings of the National Academy of Sciences of the United States of America

    (1999)
  • G.M. Edelman

    The remembered present

    (1989)
  • G.M. Edelman

    Naturalizing consciousness: A theoretical framework

    Proceedings of the National Academy of Sciences of the United States of America

    (2003)
  • G.M. Edelman

    Wider than the sky: The phenomenal gift of consciousness

    (2004)
  • Edelman, D. B., Baars, B. J., & Seth, A. K. (this volume). Identifying the hallmarks of consciousness in non-mammalian...
  • G.M. Edelman et al.

    A universe of consciousness: How matter becomes imagination

    (2000)
  • W.J. Freeman et al.

    A neurobiological theory of meaning in perception part V: Multicortical patterns of phase modulation in gamma EEG

    International Journal of Bifurcation and Chaos

    (2003)
  • P. Fries et al.

    Modulation of oscillatory neuronal synchronization by selective visual attention

    Science

    (2001)
  • J.M. Fuster

    Synopsis of function and dysfunction of the frontal lobe

    Acta Psychiatrica Scandinavica. Supplementum

    (1999)
  • M.S. Gazzaniga et al.

    Observations on visual perception after disconnexion of the cerebral hemispheres in man

    Brain

    (1965)
  • C.M. Gray et al.

    Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex

    Proceedings of the National Academy of Sciences of the United States of America

    (1989)
  • D.R. Griffin

    Animal minds: Beyond cognition to consciousness

    (2001)
  • Cited by (0)

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