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Research Article

Cerebral coherence between communicators marks the emergence of meaning

Arjen Stolk, Matthijs L. Noordzij, Lennart Verhagen, Inge Volman, Jan-Mathijs Schoffelen, Robert Oostenveld, Peter Hagoort, and Ivan Toni
  1. aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
  2. bDepartment of Cognitive Psychology and Ergonomics, University of Twente, 7500 AE Enschede, The Netherlands;
  3. cDepartment of Experimental Psychology, University of Oxford, OX1 3UD Oxford, United Kingdom;
  4. dBehavioural Science Institute, Radboud University, 6500 HE Nijmegen, The Netherlands; and
  5. eMax Planck Institute for Psycholinguistics, 6500 AH Nijmegen, The Netherlands

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PNAS December 23, 2014 111 (51) 18183-18188; first published December 8, 2014; https://doi.org/10.1073/pnas.1414886111
Arjen Stolk
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
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  • For correspondence: a.stolk@donders.ru.nl
Matthijs L. Noordzij
bDepartment of Cognitive Psychology and Ergonomics, University of Twente, 7500 AE Enschede, The Netherlands;
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Lennart Verhagen
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
cDepartment of Experimental Psychology, University of Oxford, OX1 3UD Oxford, United Kingdom;
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Inge Volman
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
dBehavioural Science Institute, Radboud University, 6500 HE Nijmegen, The Netherlands; and
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Jan-Mathijs Schoffelen
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
eMax Planck Institute for Psycholinguistics, 6500 AH Nijmegen, The Netherlands
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Robert Oostenveld
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
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Peter Hagoort
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
eMax Planck Institute for Psycholinguistics, 6500 AH Nijmegen, The Netherlands
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Ivan Toni
aDonders Institute for Brain, Cognition and Behaviour, Radboud University, 6500 HB Nijmegen, The Netherlands;
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  1. Edited by Asif A. Ghazanfar, Princeton University, Princeton, NJ, and accepted by the Editorial Board October 31, 2014 (received for review August 4, 2014)

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Significance

Building on recent electrophysiological evidence showing that novel communicative behavior relies on computations that operate over temporal scales independent from transient sensorimotor behavior, here we report that those computations occur simultaneously in pairs with a shared communicative history, but not in pairs without a shared history. This pair-specific interpersonal synchronization was driven by communicative episodes in which communicators needed to mutually adjust their conceptualizations of a signal’s use. That interpersonal cerebral synchronization was absent when communicators used stereotyped signals. These findings indicate that establishing mutual understanding is implemented through simultaneous in-phase coordination of cerebral activity across communicators, consistent with the notion that pair members temporally synchronize their conceptualizations of a signal’s use.

Abstract

How can we understand each other during communicative interactions? An influential suggestion holds that communicators are primed by each other’s behaviors, with associative mechanisms automatically coordinating the production of communicative signals and the comprehension of their meanings. An alternative suggestion posits that mutual understanding requires shared conceptualizations of a signal’s use, i.e., “conceptual pacts” that are abstracted away from specific experiences. Both accounts predict coherent neural dynamics across communicators, aligned either to the occurrence of a signal or to the dynamics of conceptual pacts. Using coherence spectral-density analysis of cerebral activity simultaneously measured in pairs of communicators, this study shows that establishing mutual understanding of novel signals synchronizes cerebral dynamics across communicators’ right temporal lobes. This interpersonal cerebral coherence occurred only within pairs with a shared communicative history, and at temporal scales independent from signals’ occurrences. These findings favor the notion that meaning emerges from shared conceptualizations of a signal’s use.

  • social interaction
  • theory of mind
  • experimental semiotics
  • dual functional magnetic resonance imaging
  • conceptual knowledge

Footnotes

  • ↵1A.S. and M.L.N. contributed equally to this work.

  • ↵2To whom correspondence should be addressed. Email: a.stolk{at}donders.ru.nl.
  • Author contributions: M.L.N. and I.T. designed research; M.L.N. and I.V. performed research; A.S. contributed new reagents/analytic tools; A.S., M.L.N., L.V., J.-M.S., R.O., and I.T. analyzed data; and A.S., L.V., P.H., and I.T. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. A.A.G. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1414886111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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How minds meet
Arjen Stolk, Matthijs L. Noordzij, Lennart Verhagen, Inge Volman, Jan-Mathijs Schoffelen, Robert Oostenveld, Peter Hagoort, Ivan Toni
Proceedings of the National Academy of Sciences Dec 2014, 111 (51) 18183-18188; DOI: 10.1073/pnas.1414886111

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How minds meet
Arjen Stolk, Matthijs L. Noordzij, Lennart Verhagen, Inge Volman, Jan-Mathijs Schoffelen, Robert Oostenveld, Peter Hagoort, Ivan Toni
Proceedings of the National Academy of Sciences Dec 2014, 111 (51) 18183-18188; DOI: 10.1073/pnas.1414886111
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Proceedings of the National Academy of Sciences: 111 (51)
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