Functional network antagonism and consciousness

Athena Demertzi; Aaron Kucyi; Adrián Ponce-Alvarez; Georgios A Keliris; Susan Whitfield-Gabrieli; Gustavo Deco

doi:10.1162/netn_a_00244

Functional network antagonism and consciousness

Netw Neurosci. 2022 Oct 1;6(4):998-1009. doi: 10.1162/netn_a_00244. eCollection 2022.

Authors

Athena Demertzi^{1

2

3

4}, Aaron Kucyi⁵, Adrián Ponce-Alvarez⁶, Georgios A Keliris⁷, Susan Whitfield-Gabrieli^{5

8}, Gustavo Deco^{6

9

10

11}

Affiliations

¹ Physiology of Cognition, GIGA Consciousness Research Unit, GIGA Institute (B34), Sart Tilman, University of Liège, Liège, Belgium.
² Psychology and Neuroscience of Cognition (PsyNCog), Faculty of Psychology, Logopedics and Educational Sciences, Sart Tilman, University of Liège, Liège, Belgium.
³ GIGA-CRC In Vivo Imaging, Sart Tilman, University of Liège, Liège, Belgium.
⁴ Fund for Scientific Research, FNRS, Bruxelles, Belgium.
⁵ Department of Psychology, Northeastern University, Boston, MA, USA.
⁶ Center for Brain and Cognition, Computational Neuroscience Group, Department of Information and Communication Technologies, Universitat Pompeu Fabra, Barcelona, Spain.
⁷ Bio-Imaging Lab, Department of Biomedical Sciences, University of Antwerp, Wilrijk, Belgium.
⁸ Northeastern University Biomedical Imaging Center (NUBIC), Northeastern University Interdisciplinary Science and Engineering Complex (ISEC), Boston, MA, USA.
⁹ Institució Catalana de la Recerca i Estudis Avançats (ICREA), Barcelona, Spain.
¹⁰ Department of Neuropsychology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
¹¹ Turner Institute for Brain and Mental Health, School of Psychological Sciences, and Monash Biomedical Imaging, Monash University, Clayton, Melbourne, VIC, Australia.

Abstract

Spontaneous brain activity changes across states of consciousness. A particular consciousness-mediated configuration is the anticorrelations between the default mode network and other brain regions. What this antagonistic organization implies about consciousness to date remains inconclusive. In this Perspective Article, we propose that anticorrelations are the physiological expression of the concept of segregation, namely the brain's capacity to show selectivity in the way areas will be functionally connected. We postulate that this effect is mediated by the process of neural inhibition, by regulating global and local inhibitory activity. While recognizing that this effect can also result from other mechanisms, neural inhibition helps the understanding of how network metastability is affected after disrupting local and global neural balance. In combination with relevant theories of consciousness, we suggest that anticorrelations are a physiological prior that can work as a marker of preserved consciousness. We predict that if the brain is not in a state to host anticorrelations, then most likely the individual does not entertain subjective experience. We believe that this link between anticorrelations and the underlying physiology will help not only to comprehend how consciousness happens, but also conceptualize effective interventions for treating consciousness disorders in which anticorrelations seem particularly affected.

Keywords: Anticorrelations; Consciousness; Functional connectivity; Integration; Neural inhibition; Segregation.

Plain language summary

The fMRI resting paradigm can quantify brain function by surpassing communication and sophisticated setups, hence helping to infer consciousness in individuals who are unable to communicate with their environment. A particular consciousness-mediated rsfMRI configuration is that of functional anticorrelations, that is, the antagonistic relationship between a specific set of brain regions. We suggest that anticorrelations are a key physiological prior, without which consciousness cannot be supported, because the brain cannot segregate how regions get connected. We postulate that segregation is possible thanks to neural inhibition, by regulating global and local inhibitory activity. We believe that the link between anticorrelations and the underlying physiology can help not only to comprehend how consciousness happens, but also conceptualize effective interventions for treating its disorders.