What binds us? Inter-brain neural synchronization and its implications for theories of human consciousness

Neuroscience of Consciousness, 2020, 6(1): niaa010 doi: 10.1093/nc/niaa010 Research article What binds us? Inter-brain neural synchronization and its implications for theories of human consciousness 1,2† and Tom Froese 2, ,‡ * 1 Psychobiology and Neuroscience Department, Faculty of Psychology, National Autonomous University of Mexico, Mexico City, Mexico; 2Embodied Cognitive Science Unit, Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan *Correspondence address. Embodied Cognitive Science Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Okinawa, 904-0495 Japan. Tel: þ81-98-966-8711; Fax: þ81-98-966-1063; E-mail: † Ana Lucı́a Valencia, https://orcid.org/0000-0003-4971-1578 ‡ Tom Froese, https://orcid.org/0000-0002-9899-5274 Abstract The association between neural oscillations and functional integration is widely recognized in the study of human cognition. Large-scale synchronization of neural activity has also been proposed as the neural basis of consciousness. Intriguingly, a growing number of studies in social cognitive neuroscience reveal that phase synchronization similarly appears across brains during meaningful social interaction. Moreover, this inter-brain synchronization has been associated with subjective reports of social connectedness, engagement, and cooperativeness, as well as experiences of social cohesion and ‘self-other merging’. These findings challenge the standard view of human consciousness as essentially first-person singular and private. We therefore revisit the recent controversy over the possibility of extended consciousness and argue that evidence of inter-brain synchronization in the fastest frequency bands overcomes the hitherto most convincing sceptical position. If this proposal is on the right track, our understanding of human consciousness would be profoundly transformed, and we propose a method to test this proposal experimentally. Keywords: neural synchronization; hyperscanning; electroencephalography; EEG; social interaction; human mind; consciousness Introduction In social cognitive neuroscience, a shift toward embodied, enactive, and participatory approaches has started to take place, moving away from individual brains and focusing on a person’s interaction with the environment. In the context of social cognition a ‘second-person’ approach (Hari and Kujala 2009; Dumas 2011; Hasson et al. 2012; Hari et al. 2013; Schilbach et al. 2013; Redcay and Schilbach 2019) has gained popularity, emphasizing the interactive nature of human cognition (Szymanski et al. 2017; Varela et al. 2017), and even challenging the individualist notion of human experience (Thompson 2001; Hari and Kujala 2009; Torrance 2009; Dumas 2011; Kirchhoff 2014; Froese 2018; Kirchhoff and Kiverstein 2019). These approaches open the space for neuroscience to experimentally address the constitutive role of brain-to-brain relationships in shaping the mind during moment-to-moment interactions (Hari and Kujala 2009; Dumas 2011; Hasson et al. 2012; Redcay and Schilbach 2019). Important philosophical topics, such as collective intentionality (Searle et al. 1990), can therefore be revisited. However, there is also some notable resistance towards moving into this uncharted territory. Even the principal architect of the hypothesis of the extended mind, Andy Clark, has Received: 13 December 2019; Revised: 27 March 2020. Accepted: 4 April 2020 C The Author(s) 2020. Published by Oxford University Press. V This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. 1 Ana Lucı́a Valencia 2 | Valencia and Froese subjective reports of social connectedness and engagement that often accompany said findings, leads to a new outlook regarding the importance of inter-brain neural synchronization in understanding the nature of human consciousness. Oscillations, synchronization and consciousness Neural oscillations are considered to be causally responsible for information transfer and integration (Rosenblum et al. 2001; Herrmann et al. 2016) since they can change the functional interactions between areas of the brain (Varela et al. 2001; Buzsáki 2006; Sauseng and Klimesch 2008; Fries 2015; Bonnefond et al. 2017), most probably through phase synchronization (Varela et al. 2001; Ward 2003; Buzsáki 2006; Uhlhaas et al. 2009). Since the phase of an oscillation reflects the exact timing of neural activity (Singer 1993; Buzsáki 2006; Cohen 2014), phase synchronization—both within and across EEG frequency bands—represents a window of functional communication and integration between neuronal populations (Sauseng and Klimesch 2008). It is established that cognitive processes require the transient coalition of several, widely distributed, and interacting neuronal groups (Thompson and Varela 2001; Ward 2003; Siegel et al. 2012) and that this large-scale dynamical integration is accomplished precisely by phase synchronization of cell assemblies (Hebb 1949; Nicolelis et al. 1997; Rodriguez et al. 1999; Varela et al. 2001; Kelso and Engstrom 2006; Sauseng and Klimesch 2008; Kelso 2009; Tognoli and Kelso 2009; Fries 2015; Engel et al. 2016) (of course, synchronization is not the only mechanism underlying effective cognitive processing; for a discussion on importance of phase desynchronization, see Tognoli and Kelso 2009 and Varela et al. 2001). Analogously, the neural substrates of consciousness may not be localized to a single region or network of a person’s brain (Kelso 1995; Thompson and Varela 2001; Engel et al. 2016). Two decades ago, Crick and Koch (1990) suggested a link between synchronized neural oscillations and consciousness; today several authors support the claim that the neural basis of consciousness (specifically of phenomenal consciousness, i.e., the integrated flow of experience Block 1995) is likely to be at the level of large-scale interactions over several frequency bands of oscillatory neural activity (Engel et al. 1999, 2016; Buzsáki 2006; Thompson and Varela 2001; Varela et al. 2001; Ward 2003; Melloni et al. 2007; Uhlhaas et al. 2009; Revonsuo 2014). For example, Llinás suggested that our subjectivity is generated by temporally coherent neural activity (‘It binds, therefore I am’ Llinás 2001), while Engel and Singer proposed that neural synchronization could be the mechanism of different aspects of consciousness, and even what generates the global unity of the self and the world (Engel et al. 1999; Revonsuo 2014). A large number of evidence further suggest that changes in the patterns of neuronal coherence, both locally and across regions, may lead to changes in mental functioning and the contents of consciousness (Engel et al. 2016). Abnormal oscillatory synchronization (...truncated)