CORE Metadata, citation and similar papers at core.ac.uk Provided by Repositório Institucional UNIFESP 10882 • The Journal of Neuroscience, November 8, 2017 • 37(45):10882–10893 Symposium Consciousness Regained: Disentangling Mechanisms, Brain Systems, and Behavioral Responses X Johan F. Storm,1 XMe´lanie Boly,2,3 X Adenauer G. Casali,4 XMarcello Massimini,5,6 XUmberto Olcese,7,8 X Cyriel M.A. Pennartz,7,8 and XMelanie Wilke9,10,11 1Division of Physiology, Department of Molecular Medicine, Institute of Basal Medical Sciences, University of Oslo, Oslo, 0317, Norway, 2Department of Neurology, University of Wisconsin, Madison, Wisconsin, 53705, 3Department of Psychiatry, University of Wisconsin, Madison, Wisconsin, 53719, 4Institute of Science and Technology, Federal University of Sa˜o Paulo, Sa˜o Jose´ dos Campos, SP, 12231-280, Brazil, 5Department of Biomedical and Clinical Sciences Luigi Sacco, University of Milan, Milan, 20157, Italy, 6Istituto Di Ricovero e Cura a Carattere Scientifico, Fondazione Don Carlo Gnocchi ONLUS, 20162 Milano, Italy, 7Cognitive and Systems Neuroscience Group, Swammerdam Institute for Life Sciences and 8Research Priority Program Brain and Cognition, University of Amsterdam, Amsterdam, 1098XH, The Netherlands, 9Department of Cognitive Neurology, University Medicine Goettingen, Goettingen, 37075, Germany, 10German Primate Center, Leibniz Institute for Primate Research, Goettingen, 37077, Germany, and 11Leibniz Science Campus Primate Cognition, Goettingen, 37077, Germany How consciousness (experience) arises from and relates to material brain processes (the “mind-body problem”) has been pondered by thinkers for centuries, and is regarded as among the deepest unsolved problems in science, with wide-ranging theoretical, clinical, and ethical implications. Until the last few decades, this was largely seen as a philosophical topic, but not widely accepted in mainstream neuroscience. Since the 1980s, however, novel methods and theoretical advances have yielded remarkable results, opening up the field for scientific and clinical progress. Since a seminal paper by Crick and Koch (1998) claimed that a science of consciousness should first search for its neural correlates (NCC), a variety of correlates have been suggested, including both content-specific NCCs, determining particular phenomenal components within an experience, and the full NCC, the neural substrates supporting entire conscious experiences. In this review, we present recent progress on theoretical, experimental, and clinical issues. Specifically, we (1) review methodological advances that are important for dissociating conscious experience from related enabling and executive functions, (2) suggest how critically reconsideringtheroleofthefrontalcortexmayfurtherdelineateNCCs,(3)advocatetheneedforgeneral,objective,brain-basedmeasures of the capacity for consciousness that are independent of sensory processing and executive functions, and (4) show how animal studies can reveal population and network phenomena of relevance for understanding mechanisms of consciousness. Key words: brain complexity; consciousness; content-specific NCC; functional connectivity; neural correlates of consciousness; no- report paradigm; Perturbational Complexity Index; unresponsive wakefulness; vegetative state Introduction all? Why are we not simply “zombies,” responding to sensory What is consciousness? How do our inner, subjective experiences input and producing behaviors according to the laws of nature, fit into our scientific world view? Why does consciousness exist at but with no subjective experiences? Questions like these (the mind-body problem, mind versus matter, consciousness versus brain) have been pondered by thinkers Received Aug. 21, 2017; revised Sept. 26, 2017; accepted Sept. 27, 2017. for centuries, and are widely regarded as among the deepest un- This work was supported by European Union’s Horizon 2020 Research and Innovation Programme under Grant solved problems in science, called “the ultimate intellectual chal- Agreement 720270 (HBP SGA1) to M.M. who, with A.G.C., primarily wrote the section “Measuring brain complexity lenge of this new millennium” (Dehaene and Changeux, 2004) and to detect (and promote) the recovery of consciousness”; C.M.A.P. and U.O., who primarily wrote the section “The conscious rodent brain: ensemble activity and long-range correlation patterns”; and J.F.S. who primarily wrote the “the major unsolved problem in biology” (Crick, 2004) with wide- “Introduction”, the “Conclusions and perspectives” and the abstract, and edited the article; Hermann and Lilly ranging theoretical, clinical, and ethical implications. Schilling Foundation, German Research Foundation WI 4046/1-1 and the Center for Nanoscale Microscopy and Until the last few decades, the fundamental problems of con- Molecular Physiology of the Brain to M.W., who primarily wrote the section “How to disentangle content-specific sciousness were largely regarded as philosophical, but not widely NCCfromdecisionmakingandvisuomotorprocesses”;NationalInstitutesofHealth/NationalInstituteofNeurological accepted as scientific topics in mainstream neuroscience. Thus, Disorders and Stroke 1R03NS096379 to M.B., who primarily wrote the section “Are the neural correlates of consciousness mainly in the front or in the back of the cerebral cortex?”; São Paulo Research Foundation Grant 2016/08263-9 to A.G.C.; influential textbooks from that period contained little about James S. McDonnell Foundation Scholar Award 2013, EU Grant H2020-FETOPEN-2014 -2015-RIA 686764 Luminous, and these issues, and in the 46 previous annual meetings of the Society Canadian Institute for Advanced Research, Azrieli Program in Brain, Mind and Consciousness to M.M.; FLAG-ERA JTC 2015 for Neuroscience (1969–2016) there have been few symposia project CANON (cofinanced by The Netherlands Organization for Scientific Research) to U.O.; and the Norwegian Research explicitly focused on consciousness: a Society for Neuroscience Council to J.F.S. The authors M.B., A.G.C., M.M., U.O., C.M.A.P., and M.W. are listed alphabetically. The authors declare no competing financial interests. Correspondence should be addressed to Dr. Johan F. Storm, Division of Physiology, Department of Molecular Medicine, Institute of Basal Medical Sciences, University of Oslo, PO Box 1103 Blindern, Oslo, 0317, Norway. E-mail: DOI:10.1523/JNEUROSCI.1838-17.2017 [email protected]. Copyright © 2017 the authors 0270-6474/17/3710882-12$15.00/0 Storm et al. • Disentangling Neural Mechanisms of Consciousness J. Neurosci., November 8, 2017 • 37(45):10882–10893 • 10883 satellite symposium on experimental approaches to conscious- earlier findings, asking which of the reported NCCs truly repre- ness chaired by Christof Koch (1998); and a minisymposium on sent consciousness and which are merely enabling factors or con- the neural basis of consciousness chaired by Tsuchiya and Maier sequences (Miller, 2007; Dehaene and Changeux, 2011; Tsuchiya (2012). This is a paradox because the widespread interest in the et al., 2015; Koch et al., 2016b; Tononi et al., 2016). brain surely stems much from its unique ability to generate our In the four sections in this review, we present recent progress conscious experiences, including thoughts, feelings, and dreams. on theoretical, experimental, and clinical issues. Specifically, we During much of the last century, the influential behaviorist (1) review methodological advancements that are important for school in psychology regarded “introspective” reports of subjec- dissociating conscious experience from related enabling and ex- tive experiences as unscientific. Since the 1980s, however, pio- ecutive functions, (2) suggest how critically reviewing the role of neers have helped making consciousness a researchable, scientific the frontal cortex may further delineate the NCCs, (3) advocate topic; and novel methods and theoretical advances (e.g. the the need for general, objective, brain-based measures of the ca- global workspace theory (GWT)/global neuronal workspace hy- pacity for consciousness that are independent of sensory process- pothesis, and the integrated information theory of consciousness ing and executive functions, and (4) show how animal studies can (IIT)) have yielded remarkable results, opening up the field for reveal population and network phenomena of relevance for un- scientific and clinical progress (Leopold and Logothetis, 2003; derstanding mechanisms of conscious states. Owen et al., 2006; Seth et al., 2008; Dehaene and Changeux, 2011; Aru et al., 2012a; Casali et al., 2013; Hobson et al., 2014; Oizumi et al., 2014; Pennartz, 2015; Tsuchiya et al., 2015; Koch et al., How to disentangle content-specific NCC from decision 2016b; Tononi et al., 2016). making and visuomotor processes Nevertheless, some uncertainty and skepticism about the sci- A fruitful approach for finding correlates of visual consciousness entific status of this topic still remain, which may be seen as has been the use of bistable visual stimuli, where the same phys- natural, given its exceptional methodological and philosophical ical stimulus gives rise to different percepts (Leopold and Logo- challenges. Because the concept of consciousness is fundamen- thetis, 1999) and perceptual suppression/masking paradigms tally derived from our subjective perspective, it seems hard to where visual stimuli are erased from consciousness (Leopold and reconcile with science in general, which is based on objectivity, Logothetis, 1999; Kim and