Neural synchrony: Difference between revisions

Despite the growth of social cognition and cognitive neuroscience prior to the early 2000s, research into the brain neglected interpersonal processes, focusing mostly on the neural mechanisms of individuals' brains and behaviors.<ref name=":1">{{Cite journal|last1=Hasson|first1=Uri|last2=Ghazanfar|first2=Asif A.|last3=Galantucci|first3=Bruno|last4=Garrod|first4=Simon|last5=Keysers|first5=Christian|date=2012-02-01|title=Brain-to-brain coupling: a mechanism for creating and sharing a social world|journal=Trends in Cognitive Sciences|language=en|volume=16|issue=2|pages=114–121|doi=10.1016/j.tics.2011.12.007|pmid=22221820|pmc=3269540|issn=1364-6613}}</ref> Furthermore, neuroscience research that did probe social questions only investigated how social processes affect neural dynamics in a single brain.<ref name=":0">{{Cite journal|last1=Nam|first1=Chang|last2=Choo|first2=Sanghyun|last3=Huang|first3=Jiali|last4=Park|first4=Jiyoung|date=2020-09-24|title=Brain-to-Brain Neural Synchrony During Social Interactions: A Systematic Review on Hyperscanning Studies|url=https://www.researchgate.net/publication/345399364|journal=[[Applied Sciences]]|volume=10|issue=19|pages=6669|doi=10.3390/app10196669|doi-access=free}}</ref> Considering that researchers clearly recognized how interpersonal interaction was fundamental to human cognition, the paucity of social and multi-brain neuroscience research represented a tension in the field, wherein any account of the brain that did not incorporate social neural activity was incomplete.<ref name=":1" /> In response to the discrepancy between the complexity of social interaction and the single-brain focus of cognitive neuroscience, researchers called for a multi-person, interaction-oriented approach to understanding the brain.<ref name=":11" /><ref name=":1" /><ref name=":2">{{Cite journal|last1=Montague|first1=P. Read|author-link=P. Read Montague|last2=Berns|first2=Gregory S.|author-link2=Gregory S. Berns|last3=Cohen|first3=Jonathan D.|author-link3=Jonathan D. Cohen|last4=McClure|first4=Samuel M.|last5=Pagnoni|first5=Giuseppe|last6=Dhamala|first6=Mukesh|last7=Wiest|first7=Michael C.|last8=Karpov|first8=Igor|last9=King|first9=Richard D.|last10=Apple|first10=Nathan|last11=Fisher|first11=Ronald E.|date=2002|title=Hyperscanning: simultaneous fMRI during linked social interactions|url=https://pubmed.ncbi.nlm.nih.gov/12202103/|journal=NeuroImage|volume=16|issue=4|pages=1159–1164|doi=10.1006/nimg.2002.1150|issn=1053-8119|pmid=12202103|s2cid=15988039}}</ref><ref>{{Cite journal|last1=Sänger|first1=Johanna|last2=Lindenberger|first2=Ulman|last3=Müller|first3=Viktor|date=2011-11-01|title=Interactive brains, social minds|journal=Communicative & Integrative Biology|volume=4|issue=6|pages=655–663|doi=10.4161/cib.17934|issn=1942-0889|pmc=3306325|pmid=22448303}}</ref><ref name=":7">{{Cite journal|last1=Balconi|first1=Michela|last2=Vanutelli|first2=Maria E.|date=2017|title=Cooperation and Competition with Hyperscanning Methods: Review and Future Application to Emotion Domain|journal=Frontiers in Computational Neuroscience|volume=11|pages=86|doi=10.3389/fncom.2017.00086|pmid=29033810|pmc=5627061|issn=1662-5188|doi-access=free}}</ref>

As a progressively paradigmatic approach in social and affective neuroscience, neural synchrony undergirds the field's search for the brain basis of social interaction.{{cn|date<ref name=November":0" 2021}}/> Nevertheless, relevant methods and concepts continue to develop.

The study of neural synchrony is predicated on advanced neuroimaging methods, particularly hyperscanning. Coined in 2002 by Montague et al.,<ref name=":2" /> hyperscanning refers to the method of simultaneously measuring the hemodynamic or neuroelectric responses of two or more brains as they engage with the same task or stimulus.<ref name=":8">{{Cite journal|last1=Babiloni|first1=Fabio|last2=Astolfi|first2=Laura|date=2014-07-01|title=Social neuroscience and hyperscanning techniques: Past, present and future|journal=Neuroscience & Biobehavioral Reviews|series=Applied Neuroscience: Models, methods, theories, reviews. A Society of Applied Neuroscience (SAN) special issue.|language=en|volume=44|pages=76–93|doi=10.1016/j.neubiorev.2012.07.006|pmid=22917915|pmc=3522775|issn=0149-7634}}</ref><ref name=":5">{{Cite journal|last1=Mu|first1=Yan|last2=Cerritos|first2=Cindy|last3=Khan|first3=Fatima|date=2018-10-23|title=Neural mechanisms underlying interpersonal coordination: A review of hyperscanning research|url=https://onlinelibrary.wiley.com/doi/pdf/10.1111/spc3.12421|journal=Social and Personality Psychology Compass|volume=12|issue=11|doi=10.1111/spc3.12421|s2cid=150259098|issn=1751-9004}}</ref><ref name=":4">{{Cite journal|last1=Dumas|first1=G.|last2=Lachat|first2=F.|last3=Martinerie|first3=J.|last4=Nadel|first4=J.|last5=George|first5=N.|date=2011-02-01|title=From social behaviour to brain synchronization: Review and perspectives in hyperscanning|url=https://www.sciencedirect.com/science/article/pii/S1959031811000066|journal=IRBM|series=NUMÉRO SPÉCIAL : LE CERVEAU DANS TOUS SES ÉTATS|language=en|volume=32|issue=1|pages=48–53|doi=10.1016/j.irbm.2011.01.002|issn=1959-0318}}</ref> The ability to record time-locked activity from multiple brains makes hyperscanning conducive to exploring the variabilityvariation in activity across brains. It also allows experimenters to examine various aspects of neural recordings in naturalistic scenarios, from low-level stimulus processing to high-level social cognition.<ref name=":3" /> For these reasons, hyperscanning has helped foster a systematic investigation of interpersonal dynamics at the level of the brain.<ref name=":4" />

Given that neural synchrony is a relatively new area of study that affords a variety of approaches, no prevailing paradigm exists to collect, analyze, and interpret the data. Many decisions, such as imaging techniques or analysis methods, depend on the researchers’ goals. However, there are some generally agreed upon best practices when designing these experiments. For example, sample sizes of about 30 are necessary to acquire reliable and reproducible statistical ISC maps.<ref name=":9" /> Furthermore, when studying shared responses, researchers typically prefer a strong stimulus that is able to generate significant brain responses, allowing researchers to detect greater levels of neural synchrony across participants. The exception to this preference is when researchers are more interested in the individual differences that drive synchrony. In these cases, researchers should employ stimuli that are strong enough to evoke neural synchrony, yet modest enough to maintain sufficient neural variability that researchers can later relate to the variability in behavioral measures.<ref>{{Cite journal|last1=Hedge|first1=Craig|last2=Powell|first2=Georgina|last3=Sumner|first3=Petroc|date=2018-06-01|title=The reliability paradox: Why robust cognitive tasks do not produce reliable individual differences|url=https://doi.org/10.3758/s13428-017-0935-1|journal=Behavior Research Methods|language=en|volume=50|issue=3|pages=1166–1186|doi=10.3758/s13428-017-0935-1|issn=1554-3528|pmc=5990556|pmid=28726177}}</ref><ref name=":3" />

One of the biggest considerations for conducting neural synchrony studies concerns the ecological validity of the design. As an inherently social phenomenon, neural synchrony calls for multidimensional stimuli that emulate the richness of the social world.<ref name=":8" /><ref>{{Cite journal|last1=Hari|first1=Riitta|last2=Kujala|first2=Miiamaaria V.|date=2009-04-01|title=Brain Basis of Human Social Interaction: From Concepts to Brain Imaging|url=https://journals.physiology.org/doi/full/10.1152/physrev.00041.2007|journal=Physiological Reviews|volume=89|issue=2|pages=453–479|doi=10.1152/physrev.00041.2007|pmid=19342612|issn=0031-9333}}</ref> Furthermore, by nature of how it is measured - through computing the variance betweenin multiple brains' responses to a task over time - neural synchrony is particularly amenable to extended social stimuli. Ecological designs are notably difficult in most neuroimaging studies, yet they are especially important for capturing the social underpinnings of neural synchronyprocesses, and they also play to the strengths and affordances of neural synchrony approaches.

Research shows that neural synchrony is indicative of the similarity in people’s narrative recall and understanding, even for ambiguous narratives. One study demonstrated this phenomenon using [[Fritz Heider|Heider]] and [[Marianne Simmel|Simmel's]]<ref>{{Cite journal|last1=Heider|first1=Fritz|author-link=Fritz Heider|last2=Simmel|first2=Marianne|author-link2=Marianne Simmel|date=1944|title=An Experimental Study of Apparent Behavior|url=https://www.jstor.org/stable/1416950|journal=[[The American Journal of Psychology]]|volume=57|issue=2|pages=243–259|doi=10.2307/1416950|issn=0002-9556|jstor=1416950}}</ref> classic paradigm, where simple shapes move around the screen in a way that causes people to imbue the shapes with stories and social meaning.<ref>{{Cite journal|last1=Nguyen|first1=Mai|last2=Vanderwal|first2=Tamara|last3=Hasson|first3=Uri|date=2019-01-01|title=Shared understanding of narratives is correlated with shared neural responses|journal=NeuroImage|language=en|volume=184|pages=161–170|doi=10.1016/j.neuroimage.2018.09.010|pmid=30217543|pmc=6287615|issn=1053-8119}}</ref> Participants who interpreted the movement of shapes in similar ways showed greater neural synchrony in cortical brain regions. This connection between neural synchrony and similarity in comprehension reliably occurs across other types of narratives, including listening to stories and free viewing of visual content,<ref>{{Cite journal|last1=Saalasti|first1=Satu|last2=Alho|first2=Jussi|last3=Bar|first3=Moshe|last4=Glerean|first4=Enrico|last5=Honkela|first5=Timo|last6=Kauppila|first6=Minna|last7=Sams|first7=Mikko|last8=Jääskeläinen|first8=Iiro P.|date=2019-04-11|title=Inferior parietal lobule and early visual areas support elicitation of individualized meanings during narrative listening|journal=Brain and Behavior|volume=9|issue=5|pages=e01288|doi=10.1002/brb3.1288|issn=2162-3279|pmc=6520291|pmid=30977309}}</ref><ref>{{Cite journal|last1=Wilson|first1=Stephen M.|last2=Molnar-Szakacs|first2=Istvan|last3=Iacoboni|first3=Marco|date=2008-01-01|title=Beyond Superior Temporal Cortex: Intersubject Correlations in Narrative Speech Comprehension|url=https://doi.org/10.1093/cercor/bhm049|journal=Cerebral Cortex|volume=18|issue=1|pages=230–242|doi=10.1093/cercor/bhm049|pmid=17504783|issn=1047-3211}}</ref><ref name=":10" /> and it persists throughout different stages of the narrative, such as consuming the story, recalling the story, and listening to another person recall the story.<ref>{{Cite journal|last1=Zadbood|first1=A.|last2=Chen|first2=J.|last3=Leong|first3=Y.C.|last4=Norman|first4=K.A.|last5=Hasson|first5=U.|date=2017-10-01|title=How We Transmit Memories to Other Brains: Constructing Shared Neural Representations Via Communication|url=https://doi.org/10.1093/cercor/bhx202|journal=Cerebral Cortex|volume=27|issue=10|pages=4988–5000|doi=10.1093/cercor/bhx202|pmid=28922834|pmc=6057550|issn=1047-3211}}</ref><ref>{{Cite journal|last1=Chen|first1=Janice|author-link=Janice Chen|last2=Leong|first2=Yuan Chang|last3=Honey|first3=Christopher J.|last4=Yong|first4=Chung H.|last5=Norman|first5=Kenneth A.|last6=Hasson|first6=Uri|date=2017|title=Shared memories reveal shared structure in neural activity across individuals|journal=[[Nature Neuroscience]]|language=en|volume=20|issue=1|pages=115–125|doi=10.1038/nn.4450|issn=1546-1726|pmc=5191958|pmid=27918531}}</ref> Together, these findings highlight neural synchrony as a reliable neural mechanism for people'sthe convergence of people's hierarchical narrative processing, suggesting that synchrony plays a critical role in how, if, and why we see meaning in the world similarly.

For example, one study that employed a computer video game found high levels of neural synchrony - and better performance - across subjects when they played on the same team, but this effect disappeared when people played against each other or by themselves.<ref>{{Cite journal|last1=Cui|first1=Xu|last2=Bryant|first2=Daniel M.|last3=Reiss|first3=Allan L.|date=2012-02-01|title=NIRS-based hyperscanning reveals increased interpersonal coherence in superior frontal cortex during cooperation|journal=NeuroImage|language=en|volume=59|issue=3|pages=2430–2437|doi=10.1016/j.neuroimage.2011.09.003|pmid=21933717|pmc=3254802|issn=1053-8119}}</ref> Similarly, researchers that administered a puzzle solving task found neural synchrony for people when they are working as a team, yet synchrony decreased for the same people when they worked separately or watched others solve the puzzle.<ref>{{Cite journal|last1=Fishburn|first1=Frank A.|last2=Murty|first2=Vishnu P.|last3=Hlutkowsky|first3=Christina O.|last4=MacGillivray|first4=Caroline E.|last5=Bemis|first5=Lisa M.|last6=Murphy|first6=Meghan E.|last7=Huppert|first7=Theodore J.|last8=Perlman|first8=Susan B.|date=2018-09-05|title=Putting our heads together: interpersonal neural synchronization as a biological mechanism for shared intentionality|journal=Social Cognitive and Affective Neuroscience|volume=13|issue=8|pages=841–849|doi=10.1093/scan/nsy060|issn=1749-5024|pmc=6123517|pmid=30060130}}</ref> Another study using a classic [[prisoner's dilemma]] game showed that participants experienced higher neural synchrony with each other in the high-cooperation-context conditions than they did in the low-cooperation-context conditions or when they interacted with the computer.<ref>{{Cite journal|last1=Hu|first1=Yi|last2=Pan|first2=Yafeng|last3=Shi|first3=Xinwei|last4=Cai|first4=Qing|last5=Li|first5=Xianchun|last6=Cheng|first6=Xiaojun|date=2018|title=Inter-brain synchrony and cooperation context in interactive decision making|url=https://pubmed.ncbi.nlm.nih.gov/29292232/|journal=Biological Psychology|volume=133|pages=54–62|doi=10.1016/j.biopsycho.2017.12.005|issn=1873-6246|pmid=29292232|s2cid=46859640}}</ref> Subjective measures of perceived cooperativeness mediated this effect. Critically, the idea that neural synchrony is robust during cooperation, that more interactive and demanding cooperative tasks recruit greater neural synchrony, and that better cooperation often links to performancebetter measuresperformance is corroborated throughout the neural synchrony literature.<ref name=":6" /><ref name=":8" />

When presented withUsing an ambiguous social narrative, Finn et al.<ref>{{Cite journal|last1=Finn|first1=Emily S.|last2=Corlett|first2=Philip R.|last3=Chen|first3=Gang|last4=Bandettini|first4=Peter A.|last5=Constable|first5=R. Todd|date=2018-05-23|title=Trait paranoia shapes inter-subject synchrony in brain activity during an ambiguous social narrative|journal=[[Nature Communications]]|language=en|volume=9|issue=1|pages=2043|doi=10.1038/s41467-018-04387-2|issn=2041-1723|pmc=5966466|pmid=29795116|bibcode=2018NatCo...9.2043F}}</ref> report that individuals with high-trait paranoia showshowed stronger neural synchrony with each other in socially-motivated cortical regions than they did with low-trait paranoia subjects - a finding that also scales when examining the semantic and syntactic similarities of their narrative recall. Similarly, research shows that people’s [[cognitive style]]s affect their level of synchrony with each other. In response to viewing a movie, Bacha-Trams et al.<ref>{{Cite journal|last1=Bacha-Trams|first1=M.|last2=Alexandrov|first2=Y.|last3=Broman|first3=Emilia|last4=Glerean|first4=E.|last5=Kauppila|first5=Minna|last6=Kauttonen|first6=J.|last7=Ryyppö|first7=Elisa|last8=Sams|first8=M.|last9=Jääskeläinen|first9=I.|date=2018|title=A drama movie activates brains of holistic and analytical thinkers differentially|journal=Social Cognitive and Affective Neuroscience|volume=13|issue=12|pages=1293–1304|doi=10.1093/scan/nsy099|pmid=30418656|pmc=6277741|s2cid=53280358}}</ref> demonstrated that holistic thinkers showed greater neural synchrony with each other, and presumably understood the movie more similarly, than analytic thinkers did with each other. The two groups also exhibited within-group synchrony in different brain regions.

The idea that individual-level differences affect neural synchrony extends to clinical areas as well. Some research indicates that people who manage [[Autism spectrum|autism spectrum disorder]] exhibit distinct and diminished patterns of neural synchrony with other people compared to people without autism spectrum disorder.<ref>{{Cite journal|last1=Salmi|first1=J.|last2=Roine|first2=U.|last3=Glerean|first3=E.|last4=Lahnakoski|first4=J.|last5=Nieminen-von Wendt|first5=T.|last6=Tani|first6=P.|last7=Leppämäki|first7=S.|last8=Nummenmaa|first8=L.|last9=Jääskeläinen|first9=I. P.|last10=Carlson|first10=S.|last11=Rintahaka|first11=P.|date=2013-01-01|title=The brains of high functioning autistic individuals do not synchronize with those of others|journal=NeuroImage: Clinical|language=en|volume=3|pages=489–497|doi=10.1016/j.nicl.2013.10.011|pmid=24273731|pmc=3830058|issn=2213-1582}}</ref><ref>{{Cite journal|last1=Tanabe|first1=Hiroki|last2=Kosaka|first2=Hirotaka|last3=Saito|first3=Daisuke|last4=Koike|first4=Takahiko|last5=Hayashi|first5=Masamichi|last6=Izuma|first6=Keise|last7=Komeda|first7=Hidetsugu|last8=Ishitobi|first8=Makoto|last9=Omori|first9=Masao|last10=Munesue|first10=Toshio|last11=Okazawa|first11=Hidehiko|date=2012|title=Hard to "tune in": neural mechanisms of live face-to-face interaction with high-functioning autistic spectrum disorder|journal=Frontiers in Human Neuroscience|volume=6|pages=268|doi=10.3389/fnhum.2012.00268|pmid=23060772|pmc=3459004|issn=1662-5161|doi-access=free}}</ref> Clinically driven discrepancies in neural synchrony have also been shown to increase along with symptom severity.<ref>{{Cite journal|last1=Guo|first1=Christine C.|last2=Nguyen|first2=Vinh T.|last3=Hyett|first3=Matthew P.|last4=Parker|first4=Gordon B.|last5=Breakspear|first5=Michael J.|date=2015-06-26|title=Out-of-sync: disrupted neural activity in emotional circuitry during film viewing in melancholic depression|journal=Scientific Reports|language=en|volume=5|issue=1|pages=11605|doi=10.1038/srep11605|pmid=26112251|pmc=4481375|bibcode=2015NatSR...511605G|issn=2045-2322}}</ref> In clinical and scientific neuroscience, further research is needed to parse how and why people respond idiosyncratically to identical stimuli and conditions.