Consciousness and complexity

Science

Volumn 282, Issue 5395, 1998, Pages 1846-1851

  Tononi, Giulio ^a   Edelman, Gerald M ^a  

^a NEUROSCIENCES INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CONSCIOUSNESS; DATA ANALYSIS; DEPTH PERCEPTION; DIFFERENTIATION; EXPERIENCE; HYPOTHESIS; INTEGRATION; PHENOMENOLOGY; PRIORITY JOURNAL; REVIEW; TASK PERFORMANCE; VISUAL INFORMATION;

EID: 0032484086     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.282.5395.1846     Document Type: Review

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26. Lesion studies indicate that consciousness is abolished by widely distributed damage but not by localized cortical damage. The only localized brain lesions resulting in loss of consciousness typically affect the reticular core in the upper brainstem and hypothalamus or its rostral extensions in the reticular and intralaminar thalamic nuclei [F. Plum, in Normal and Altered States of Function, A. Peters and E. G. Jones, Eds. (Plenum, New York, 1991), vol. 9, p. 359]. Although it has been suggested that the reticular core may have a privileged connection to conscious experience [J. E. Bogen, Consciousness Cognit. 4, 52 (1995)], its activity may simply be required to sustain distributed activity patterns in the cortex.
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37. E. D. Lumer, G. M. Edelman, G. Tononi, Cereb. Cortex 7, 207 (1997); ibid., p. 228. For example, in a largescale model of the visual system, reentrant interactions between groups of neurons in perceptual or "posterior" areas and in executive or "anterior" areas rapidly led to their synchronous firing and to a correct behavioral discrimination. This discrimination was based on the dynamic binding of multiple visual attributes (position, movement, color, form) and of different levels of stimulus generalization (local features, invariant aspects of stimuli).
38. E. D. Lumer, G. M. Edelman, G. Tononi, Cereb. Cortex 7, 207 (1997); ibid., p. 228. For example, in a largescale model of the visual system, reentrant interactions between groups of neurons in perceptual or "posterior" areas and in executive or "anterior" areas rapidly led to their synchronous firing and to a correct behavioral discrimination. This discrimination was based on the dynamic binding of multiple visual attributes (position, movement, color, form) and of different levels of stimulus generalization (local features, invariant aspects of stimuli).
39. B. Kolb and I. Q. Whishaw, Fundamentals of Human Neuropsychology (Freeman, New York, 1996). Psychiatric dissociation syndromes and conversion disorders may originate from a similar alteration of reentrant interactions, although in these cases, the disconnection would be functional rather than anatomical [J. F. Kihlstrom, Consciousness Cognit. 1, 47 (1992)]. Some explicit-implicit dissociations, such as amnesia, may also be due to a partial disconnection of a lesioned area from the more global pattern of neural activity that is associated with consciousness [D. L. Schacter, Proc. Natl. Acad. Sci. U.S.A. 89, 11113 (1992)].
40. B. Kolb and I. Q. Whishaw, Fundamentals of Human Neuropsychology (Freeman, New York, 1996). Psychiatric dissociation syndromes and conversion disorders may originate from a similar alteration of reentrant interactions, although in these cases, the disconnection would be functional rather than anatomical [J. F. Kihlstrom, Consciousness Cognit. 1, 47 (1992)]. Some explicit-implicit dissociations, such as amnesia, may also be due to a partial disconnection of a lesioned area from the more global pattern of neural activity that is associated with consciousness [D. L. Schacter, Proc. Natl. Acad. Sci. U.S.A. 89, 11113 (1992)].
41. B. Kolb and I. Q. Whishaw, Fundamentals of Human Neuropsychology (Freeman, New York, 1996). Psychiatric dissociation syndromes and conversion disorders may originate from a similar alteration of reentrant interactions, although in these cases, the disconnection would be functional rather than anatomical [J. F. Kihlstrom, Consciousness Cognit. 1, 47 (1992)]. Some explicit-implicit dissociations, such as amnesia, may also be due to a partial disconnection of a lesioned area from the more global pattern of neural activity that is associated with consciousness [D. L. Schacter, Proc. Natl. Acad. Sci. U.S.A. 89, 11113 (1992)].
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69. 1) - I(X) [G. Tononi, G. M. Edelman, O. Sporns, Trends Cognit. Sci., in press]. Note that complexity measures should be applied to a single system (a functional cluster) and not to a collection of independent or nearly independent subsystems.
70. 1) - I(X) [G. Tononi, G. M. Edelman, O. Sporns, Trends Cognit. Sci., in press]. Note that complexity measures should be applied to a single system (a functional cluster) and not to a collection of independent or nearly independent subsystems.
71. Changes in complexity can be obtained without modifying the anatomical connectivity of the model by simulating the transition between the burst-pause pattern of firing typical of slow-wave sleep and the tonic mode of firing typical of waking and REM sleep (G. Tononi, unpublished material). It should be noted that high complexity is not easy to achieve. A system of elements that are randomly interconnected, for instance, may look very complicated, but it has low values of complexity. On the other hand, systems that undergo selective processes so as to match the statistical structure of a rich environment will gradually increase their complexity [G. Tononi, O. Sporns, G. M. Edelman, Proc. Natl. Acad. Sci. U.S.A. 93, 3422 (1996)].
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75. D. A. Leopold and N. K. Logothetis, Nature 379, 549 (1996); D. L. Shenberg and N. K. Logothetis, Proc. Natl. Acad. Sci. U.S.A. 94, 3408 (1997). For other instances of dissociation, see (26); M. Gur and D. M. Snodderly, Vision Res. 37, 377 (1997); I. N. Pigarev, H. C. Nothdurft, S. Kastner, Neuroreport 8, 2557 (1997); D. C. Bradley, G. C. Chang, R. A. Andersen, Nature 392, 714 (1998).
76. D. A. Leopold and N. K. Logothetis, Nature 379, 549 (1996); D. L. Shenberg and N. K. Logothetis, Proc. Natl. Acad. Sci. U.S.A. 94, 3408 (1997). For other instances of dissociation, see (26); M. Gur and D. M. Snodderly, Vision Res. 37, 377 (1997); I. N. Pigarev, H. C. Nothdurft, S. Kastner, Neuroreport 8, 2557 (1997); D. C. Bradley, G. C. Chang, R. A. Andersen, Nature 392, 714 (1998).
77. D. A. Leopold and N. K. Logothetis, Nature 379, 549 (1996); D. L. Shenberg and N. K. Logothetis, Proc. Natl. Acad. Sci. U.S.A. 94, 3408 (1997). For other instances of dissociation, see (26); M. Gur and D. M. Snodderly, Vision Res. 37, 377 (1997); I. N. Pigarev, H. C. Nothdurft, S. Kastner, Neuroreport 8, 2557 (1997); D. C. Bradley, G. C. Chang, R. A. Andersen, Nature 392, 714 (1998).
78. D. A. Leopold and N. K. Logothetis, Nature 379, 549 (1996); D. L. Shenberg and N. K. Logothetis, Proc. Natl. Acad. Sci. U.S.A. 94, 3408 (1997). For other instances of dissociation, see (26); M. Gur and D. M. Snodderly, Vision Res. 37, 377 (1997); I. N. Pigarev, H. C. Nothdurft, S. Kastner, Neuroreport 8, 2557 (1997); D. C. Bradley, G. C. Chang, R. A. Andersen, Nature 392, 714 (1998).
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80. D. J. Simons and D. T. Levin, Trends Cogn. Sci. 1, 261 (1997). The neurological evidence is in agreement with these psychological observations. In the adult, lesions of the retina produce blindness, but they do not eliminate visual imagery, visual memories, and visual dreams, while the latter are eliminated by lesions of certain visual cortical areas [M. Solms, The Neuropsychology of Dreams (Erlbaum, Mahwah, NJ, 1997)]. V1 may be important, however, to provide visual consciousness with a certain degree of detail. See also R. Jackendoff [Consciousness and the Computational Mind (MIT Press, Cambridge, MA, 1987)].
81. D. J. Simons and D. T. Levin, Trends Cogn. Sci. 1, 261 (1997). The neurological evidence is in agreement with these psychological observations. In the adult, lesions of the retina produce blindness, but they do not eliminate visual imagery, visual memories, and visual dreams, while the latter are eliminated by lesions of certain visual cortical areas [M. Solms, The Neuropsychology of Dreams (Erlbaum, Mahwah, NJ, 1997)]. V1 may be important, however, to provide visual consciousness with a certain degree of detail. See also R. Jackendoff [Consciousness and the Computational Mind (MIT Press, Cambridge, MA, 1987)].
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86. A. D. Milner, Neuropsychologia 33, 1117 (1995); _ and M. A. Goodale, The Visual Brain in Action (Oxford Univ. Press, New York, 1995).
87. The organization of the anatomical connectivity of certain brain regions, such as the thalamocortical system, is much more effective in generating coherent dynamic states than that of other regions, such as the cerebellum or the basal ganglia (G. Tononi, unpublished material). Consistent with this, although in cortical and thalamic areas 20 to 50% of all pairs of neurons recorded are broadly synchronized, neurons in the internal segment of the globus pallidus, the output station of the basal ganglia, are almost completely uncorrelated [H. Bergman et al., Trends Neurosci. 21, 32 (1998)].
88. The organization of the anatomical connectivity of certain brain regions, such as the thalamocortical system, is much more effective in generating coherent dynamic states than that of other regions, such as the cerebellum or the basal ganglia (G. Tononi, unpublished material). Consistent with this, although in cortical and thalamic areas 20 to 50% of all pairs of neurons recorded are broadly synchronized, neurons in the internal segment of the globus pallidus, the output station of the basal ganglia, are almost completely uncorrelated [H. Bergman et al., Trends Neurosci. 21, 32 (1998)].
89. If the fast integration of neural activity comes at a premium in terms of number of connections and energetic requirements, neuronal groups in "higher" areas should be privileged members of the dynamic core underlying consciousness. Everything else being equal, their firing is more informative, in the sense that it rules out a larger number of possibilities. For example, the firing of face-selective neurons in area IT considerably reduces uncertainty about a visual scene (seeing a face rules out countless other visual scenes), while the firing of retinal neurons reduces uncertainty by much less (a bright spot in a certain position of the visual field is consistent with countless visual scenes). The results of studies of binocular rivalry in monkeys and humans mentioned above are consistent with this view.
90. We emphasize that the dynamic core, the highly complex, rapidly established functional cluster proposed to underlie conscious experience, is in no way the only integrated but distributed neural process that is relevant to brain function. We have hypothesized that distributed but integrated neural processes called global mappings, encompassing portions of the thalamocortical system, as well as parallel loops through cortical appendages such as the basal ganglia, the hippocampus, and the cerebellum, underlie the unity of behavioral sequences (4). The functional integration of global mappings is envisioned to occur at longer time scales than the dynamic core (seconds as opposed to fractions of a second). However, these two kinds of dynamic processes are expected to partially overlap for short periods of time.
91. Qualia - the seemingly inexplicable phenomenological manifestations of conscious experience - are conceived within this framework as rapid, highly informative discriminations within a repertoire of billions of neural states available to a unified neural process of great complexity. They correspond to the generation of a large amount of information in a short period of time. In this view, each quale - even a seemingly simple quale like a feeling of "redness" -corresponds to a discriminable state of the dynamic core in its entirety, and not merely to the state of a specific group of neurons in a certain brain area. The subjective meaning or quale of "redness," for example, would be defined by the (increased) activity of red-selective neurons as much as by the (reduced or unmodified) activity of neuronal groups selective for green or blue, for visual motion or shape, for auditory or somatosensory events, and for proprioceptive inputs, body schemas, emotions, intentions, and so forth, that jointly constitute the dynamic core. This view is antithetical to modular or atomistic approaches to consciousness (2).
92. E. Vaadia et al., Nature 373, 515 (1995).
93. E. Seidemann, I. Meilijson, M. Abeles, H. Bergman, E. Vaadia, J. Neurosci. 16, 752 (1996).
94. It is perhaps worth pointing out that our analysis predicts the possibility of constructing a conscious artifact and outlines some key principles that should constrain its construction. This work was carried out as part of the theoretical neurobiology program at The Neurosciences Institute, which is supported by Neurosciences Research Foundation. The Foundation receives major support for this program from Novartis Pharmaceutical Corporation and the W. M. Keck Foundation.