A New Approach to the Study of Consciousness from the Theory of Integrated Information Point of View (Review)
The continuously increasing number of patients with chronic disorders of consciousness results in a growing need for an objective method of evaluating the level of consciousness in this category of patients in the clinical practice of neurologists and critical care physicians. One of the up-to-date approaches is based on the integrated information theory (IITC; Tononi, 2004, 2012, 2014). According to this theory the mechanisms determining the state of consciousness are integrally connected with certain conceptually coordinated structures that are closely interrelated with each other, and exist independently of external influences. On the basis of this theory Casali et al. (2013) developed approaches to the quantitative evaluation of integrated information in the neuronal system that depend on cause-and-effect relationships between its different elements. As a result, the term ‘perturbational complexity index’ has been introduced in respect of consciousness. It allows measurement of the integrity and spatio-temporal structure of the pattern of cortical excitation caused by non-invasive stimulation of the brain cortex, and, therefore, a description of the degree of complexity of the electrical signals in the brain. The values of this index differ in various states of consciousness (e.g., wakefulness, deep sleep, anesthesia, vegetative state etc.) that supports its use in patients with chronic disorders of consciousness as a new diagnostic tool.
- van Erp W.S., Lavrijsen J.C., van de Laar F.A., Vos P.E., Laureys S., Koopmans R.T. The vegetative state/unresponsive wakefulness syndrome: a systematic review of prevalence studies. Eur J Neurol 2014; 21(11): 1361–1368, https://doi.org/10.1111/ene.12483.
- Giacino J.T., Ashwal S., Childs N., Cranford R., Jennett B., Katz D.I., Kelly J.P., Rosenberg J.H., Whyte J., Zafonte R.D., Zasler N.D. The minimally conscious state: definition and diagnostic criteria. Neurology 2002; 58(3): 349–353, https://doi.org/10.1212/WNL.58.3.349.
- Cruse D.,
Chennu S.,Chatelle C., Bekinschtein T.A., Fernández-Espejo D., Pickard J.D., Laureys S., Owen A.M. Bedside detection of awareness in the vegetative state: a cohort study. Lancet 2011; 378(9809): 2088–2094, https://doi.org/10.1016/S0140-6736(11)61224-5. - Childs N.L., Mercer W.N., Childs H.W. Accuracy of diagnosis of persistent vegetative state. Neurology 1993; 43(8): 1465–1465, https://doi.org/10.1212/wnl.43.8.1465.
- Andrews K., Murphy L., Munday R., Littlewood C. Misdiagnosis of the vegetative state:
retrospective study in a rehabilitation unit. BMJ 1996; 313(7048): 13–16, https://doi.org/10.1136/bmj.313.7048.13. - Schnakers C., Giacino J., Kalmar K.,
Piret S., Lopez E., Boly M., Malone R., Laureys S. Does the FOUR score correctly diagnose the vegetative and minimally conscious states? Ann Neurol 2006; 60(6): 744–745, https://doi.org/10.1002/ana.20919. - Schnakers C., Vanhaudenhuyse A., Giacino J., Ventura M., Boly M., Majerus S., Moonen G., Laureys S. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 2009; 9(1), https://doi.org/10.1186/1471-2377-9-35.
- Crone J.S., Ladurner G., Höller Y., Golaszewski S., Trinka E., Kronbichler M. Deactivation of the default mode network as a marker of impaired consciousness: an fMRI study. PLoS One 2011; 6(10): e26373, https://doi.org/10.1371/journal.pone.0026373.
- Ragazzoni A.,
Pirulli C., Veniero D.,Feurra M., Cincotta M.,Giovannelli F., Chiaramonti R., Lino M., Rossi S., Miniussi C. Vegetative versus minimally conscious states: a study using TMS-EEG, sensory and event-related potentials. PLoS One 2013; 8(2): e57069, https://doi.org/10.1371/journal.pone.0057069. - Rosanova M., Gosseries O., Casarotto S., Boly M., Casali A.G., Bruno M.-A., Mariotti M., Boveroux P., Tononi G., Laureys S., Massimini M. Recovery of cortical effective connectivity and recovery of consciousness in vegetative patients. Brain 2012; 135(4): 1308–1320, https://doi.org/10.1093/brain/awr340.
- King J.R., Faugeras F., Gramfort A.,
Schurger A., El Karoui I., Sitt J.D., Rohaut B., Wacongne C.,Labyt E., Bekinschtein T., Cohen L., Naccache L., Dehaene S. Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness. NeuroImage 2013; 83: 726–738, https://doi.org/10.1016/j.neuroimage.2013.07.013. - Perrin F., Schnakers C., Schabus M., Degueldre C., Goldman S., Brédart S., Faymonville M.E., Lamy M., Moonen G., Luxen A., Maquet P., Laureys S. Brain response to one’s own name in vegetative state, minimally conscious state, and locked-in syndrome. Arch Neurol 2006; 63(4): 562–569, https://doi.org/10.1001/archneur.63.4.562.
- Seth A.K., Dienes Z., Cleeremans A., Overgaard M., Pessoa L. Measuring consciousness: relating
behavioural and neurophysiological approaches. Trends Cogn Sci 2008; 12(8): 314–321, https://doi.org/10.1016/j.tics.2008.04.008. - Rees G., Frith C. Methodologies for identifying the neural correlates of consciousness. In: The
blackwell companion to consciousness. USA: Blackwell Publishing, Malden; 2007; p. 551–566, https://doi.org/10.1002/9780470751466.ch44. - Owen A.M. Detecting consciousness: a unique role for neuroimaging. Annu Rev Psychol 2013; 64(1): 109–133, https://doi.org/10.1146/annurev-psych-113011-143729.
- Jox R.J., Bernat J.L., Laureys S., Racine E. Disorders of consciousness: responding to requests for novel diagnostic and therapeutic interventions. Lancet Neurol 2012; 11(8): 732–738, https://doi.org/10.1016/s1474-4422(12)70154-0.
- Posner J.B., Saper C.B., Schiff N.D., Plum F. Plum and Posner’s diagnosis of stupor and coma. Oxford University Press; 2007, https://doi.org/10.1093/med/9780195321319.001.0001.
- Zeman A. Consciousness. Brain 2001; 124(7): 1263–1289, https://doi.org/10.1093/brain/124.7.1263.
- Laureys S. The neural correlate of (un)awareness: lessons from the vegetative state. Trends Cogn Sci 2005; 9(12): 556–559, https://doi.org/10.1016/j.tics.2005.10.010.
- Moruzzi G., Magoun H.W. Brain stem reticular formation and activation of the EEG. Electroencephalogr Clin Neurophysiol 1949; 1(4): 455–473, https://doi.org/10.1016/0013-4694(49)90219-9.
- Munk M.H.J., Roelfsema P.R., Konig P., Engel A.K., Singer W. Role of reticular activation in the modulation of intracortical synchronization. Science 1996; 272(5259): 271–274, https://doi.org/10.1126/science.272.5259.271.
- Wilkinson D., Savulescu J. Is it better to be minimally conscious than vegetative? J Med Ethics 2012; 39(9): 557–558, https://doi.org/10.1136/medethics-2012-100954.
- Giacino J.T., Kalmar K., Whyte J. The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004; 85(12): 2020–2029, https://doi.org/10.1016/j.apmr.2004.02.033.
- Cairns H., Oldfield R.C., Pennybacker J.B., Whitteridge D. Akinetic mutism with an epidermoid cyst of the 3rd ventricle. Brain 1941; 64(4): 273–290, https://doi.org/10.1093/brain/64.4.273.
- Courjon J., Naquet R.,
Baurand C., Chamant J., Choux M., Gerin P., Lang M., Revol M., Vigouroux R.P. Diagnostic and prognostic value of the EEG in the immediate aftermath of cranial trauma. Rev Electroencephalogr Neurophysiol Clin 1971; 1(2): 133–150. - Practice parameters: assessment and management of patients in the persistent vegetative state (summary statement). Neurology 1995; 45(5): 1015–1018, https://doi.org/10.1212/wnl.45.5.1015.
- Jennett B., Plum F. Persistent vegetative state after brain damage. Lancet 1972; 299(7753): 734–737, https://doi.org/10.1016/s0140-6736(72)90242-5.
- Laureys S.,
Celesia G.G., Cohadon F., Lavrijsen J., León-Carrión J.,Sannita W.G., Sazbon L., Schmutzhard E., von Wild K.R., Zeman A., Dolce G.; European Task Force on Disorders of Consciousness. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010; 8(1), https://doi.org/10.1186/1741-7015-8-68. - Plum F. Coma and related global disturbances of the human conscious state. Cerebral Cortex 1991; 359–425, https://doi.org/10.1007/978-1-4615-6622-9_9.
- The Multi-Society Task Force on PVS. Medical aspects of the persistent vegetative state. N Engl J Med 1994; 330(21): 1499–1508, https://doi.org/10.1056/nejm199405263302107.
- Rosenthal D.M. Consciousness and mind. Oxford: Oxford University Press; 2005.
- Melloni L., Molina C., Pena M., Torres D., Singer W., Rodriguez E. Synchronization of neural activity across cortical areas correlates with conscious perception. J Neurosci 2007; 27(11): 2858–2865, https://doi.org/10.1523/jneurosci.4623-06.2007.
- Sherman S.M.,
Guillery R.W. The role of the thalamus in the flow of information to the cortex. Philos Trans R Soc Lond B Biol Sci 2002; 357(1428): 1695–1708, https://doi.org/10.1098/rstb.2002.1161. - Seth A.K. The grand challenge of consciousness. Front Psychol 2010, https://doi.org/10.3389/fpsyg.2010.00005.
- McCulloch W.S., Pitts W. A logical calculus of the ideas immanent in nervous activity. Bull Math Biol 1943; 5(4): 115–133, https://doi.org/10.1007/bf02478259.
- Mountcastle V.B. Modality and topographic properties of single neurons of cat’s somatic sensory cortex. J Neurophysiol 1957; 20(4): 408–434.
- Hubel D.H., Wiesel T.N. Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J Physiol 1962; 160(1): 106–154, https://doi.org/10.1113/jphysiol.1962.sp006837.
- Hebb D.O. The organization of behavior. New York: Wiley; 1949.
- Searle J. The mystery of consciousness. New York; 1997.
- Edelman G.M., Mountcastle V. The mindful brain: cortical organization and the group-selective theory of higher brain functions. Cambridge: MIT Press; 1978.
- Edelman G.M. The remembered present. A biological theory of consciousness. New York: Basics Books; 1989.
- Edelman G.M. Neural
darwinism . The theory of neuronal group selection. New York: BasicBooks; 1987. - Edelman G.M. Naturalizing consciousness: a theoretical framework. Proc Natl Acad Sci USA 2003; 100(9): 5520–5524, https://doi.org/10.1073/pnas.0931349100.
- Mountcastle V. The columnar organization of the neocortex. Brain 1997; 120(4): 701–722, https://doi.org/10.1093/brain/120.4.701.
- Edelman G.M., Tononi G. A universe of consciousness: how matter becomes imagination. New York: Basic Books; 2000.
- Tononi G., Edelman G.M. Consciousness and complexity. Science 1998; 282(5395): 1846–1851, https://doi.org/10.1126/science.282.5395.1846.
- Tononi G., Sporns O., Edelman G.M. A measure for brain complexity: relating functional segregation and integration in the nervous system. Proc Natl Acad Sci USA 1994; 91(11): 5033–5037, https://doi.org/10.1073/pnas.91.11.5033.
- Tononi G., Sporns O., Edelman G.M. Reentry and the problem of integrating multiple cortical areas: simulation of dynamic integration in the visual system. Cerebral Cortex 1992; 2(4): 310–335, https://doi.org/10.1093/cercor/2.4.310.
- Zeki S. A vision of the brain. Oxford: Blackwell Scientific Publications; 1993.
- Tong F., Engel S.A. Interocular rivalry revealed in the human cortical blind-spot representation. Nature 2001; 411(6834): 195–199, https://doi.org/10.1038/35075583.
- Jones E.G. A new view of specific and nonspecific thalamocortical connections. Adv Neurol 1998; 77: 49–73.
- Tallon-Baudry C. On the neural mechanisms subserving consciousness and attention. Front Psychol 2012; 2, https://doi.org/10.3389/fpsyg.2011.00397.
- Llinas R., Ribary U., Contreras D., Pedroarena C. The neuronal basis for consciousness. Philos Trans R Soc Lond B Biol Sci 1998; 353(1377): 1841–1849, https://doi.org/10.1098/rstb.1998.0336.
- Crick F., Koch C. A framework for consciousness. Nat Neurosci 2003; 6(2): 119–126, https://doi.org/10.1038/nn0203-119.
- Crick F., Koch C. Some reflections on visual awareness. Cold Spring Harb Symp Quant Biol 1990; 55: 953–962, https://doi.org/10.1101/sqb.1990.055.01.089.
- Crick F., Koch C. Are we aware of neural activity in primary visual cortex? Nature 1995; 375(6527): 121–123, https://doi.org/10.1038/375121a0.
- Crick F.C., Koch C. What is the function of the claustrum? Philos Trans R Soc Lond B Biol Sci 2005; 360(1458): 1271–1279, https://doi.org/10.1098/rstb.2005.1661.
- Van Gaal S., Lamme V.A.F. Unconscious high-level information processing: implication for neurobiological theories of consciousness. Neuroscientist 2011; 18(3): 287–301, https://doi.org/10.1177/1073858411404079.
- Shannon C.E. A mathematical theory of communication. Bell System Technical Journal 1948; 27(4): 623–656, https://doi.org/10.1002/j.1538-7305.1948.tb00917.x.
- Колмогоров А.Н. Три подхода к определению понятия «количество информации». Проблемы передачи информации 1965; 1(1): 3–11. Kholmogorov A.N. Three approaches to the definition of “the quantity of information”. Problemy peredachi informatsii 1965; 1(1): 3–11.
- Tononi G., Sporns O., Edelman G.M. A complexity measure for selective matching of signals by the brain. Proc Natl Acad Sci USA 1996; 93(8): 3422–3427, https://doi.org/10.1073/pnas.93.8.3422.
- Seth A.K., Barrett A.B., Barnett L. Causal density and integrated information as measures of conscious level. Philos Trans A Math Phys Eng Sci 2011; 369(1952): 3748–3767, https://doi.org/10.1098/rsta.2011.0079.
- Kotchoubey B. Event-related potential measures of consciousness: two equations with three unknowns. Prog Brain Res 2005; 150: 427–444, https://doi.org/10.1016/s0079-6123(05)50030-x.
- Ilmoniemi R.J., Virtanen J., Ruohonen J., Karhu J.,
Aronen H.J., Näätänen R., Katila T. Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. NeuroReport 1997; 8(16): 3537–3540, https://doi.org/10.1097/00001756-199711100-00024. - Lempel A., Ziv J. On the complexity of finite sequences. IEEE Trans Inf Theory 1976; 22(1): 75–81, https://doi.org/10.1109/tit.1976.1055501.
- Tononi G. An information integration theory of consciousness. BMC Neurosci 2004; 5: 42, https://doi.org/10.1186/1471-2202-5-42.
- Tononi G. Integrated information theory of consciousness: an updated account. Archives Italiennes de Biologie 2012; (2–3): 56–90.
- Oizumi M., Albantakis L., Tononi G. From the phenomenology to the mechanisms of consciousness: Integrated Information Theory 3.0. PLoS Comput Biol 2014; 10(5): e1003588, https://doi.org/10.1371/journal.pcbi.1003588.
- Mudrik L., Breska A., Lamy D., Deouell L.Y. Integration without awareness: expanding the limits of unconscious processing. Psychol Sci 2011; 22(6): 764–770, https://doi.org/10.1177/0956797611408736. Tononi G. Information measures for conscious experience. Arch Ital Biol 2001; 139(4): 367–371.
- Tononi G. Consciousness and the brain: theoretical aspects. In: Encyclopedia of neuroscience. Adelman G., Smith B. (editors). Amsterdam: Elsevier; 2004.
- Tononi G., Sporns O. Measuring information integration. BMC Neurosci 2003; 4(1): 31, https://doi.org/10.1186/1471-2202-4-31.
- Cerullo M.A. The problem with Phi: a critique of integrated information theory. PLoS Comput Biol 2015; 11(9): e1004286, https://doi.org/10.1371/journal.pcbi.1004286.
- Rosanova M., Casali A., Bellina V., Resta F., Mariotti M., Massimini M. Natural frequencies of human corticothalamic circuits. J Neurosci 2009; 29(24): 7679–7685, https://doi.org/10.1523/jneurosci.0445-09.2009.
- Casali A.G., Gosseries O., Rosanova M., Boly M., Sarasso S., Casali K.R., Casarotto S., Bruno M.A., Laureys S., Tononi G., Massimini M. A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 2013; 5(198): 198ra105–198ra105, https://doi.org/10.1126/scitranslmed.3006294.
- Koch C., Massimini M., Boly M., Tononi G. Neural correlates of consciousness: progress and problems. Nat Rev Neurosci 2016; 17(5): 307–321, https://doi.org/10.1038/nrn.2016.22.
- Leopold D.A. Primary visual cortex: awareness and blindsight. Annu Rev Neurosci 2012; 35(1): 91–109, https://doi.org/10.1146/annurev-neuro-062111-150356.
- Engel A.K., Singer W. Temporal binding and the neural correlates of sensory awareness. Trends Cogn Sci 2001; 5(1): 16–25, https://doi.org/10.1016/s1364-6613(00)01568-0.
- Sklar A.Y., Levy N., Goldstein A., Mandel R., Maril A., Hassin R.R. Reading and doing arithmetic nonconsciously. Proc Natl Acad Sci USA 2012; 109(48): 19614–19619, https://doi.org/10.1073/pnas.1211645109.
- Chalmers D. Facing up to the problem of consciousness. Journal of Consciousness Studies 1995; 2(3): 200–219.
- Sarasso S., Boly M., Napolitani M., Gosseries O., Charland-Verville V., Casarotto S., Rosanova M., Casali A.G., Brichant J.F., Boveroux P., Rex S., Tononi G., Laureys S., Massimini M. Consciousness and complexity during unresponsiveness induced by Propofol, Xenon, and Ketamine. Curr Biol 2015; 25(23): 3099–3105, https://doi.org/10.1016/j.cub.2015.10.014.