Cerebral coherence between communicators marks the emergence of meaning

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 111; no. 51; pp. 18183 - 18188
• Main Authors: Stolk, Arjen, Noordzij, Matthijs L., Verhagen, Lennart, Volman, Inge, Schoffelen, Jan-Mathijs, Oostenveld, Robert, Hagoort, Peter, Toni, Ivan
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 23.12.2014; National Acad Sciences
• Subjects: Adolescent; Adult; Anatomy; Behavior; Behavioral neuroscience; Biological Sciences; Brain; Brain - physiology; Brain Mapping; Communication; Conceptualization; Gameboards; Humans; Magnetic Resonance Imaging; Male; Modeling; Neurochemistry; Neurons; Signal transduction; Signals; Social interaction; Social Sciences; Spectrum analysis; Time series; Treaties; Young Adult; dual functional magnetic resonance imaging; social interaction; conceptual knowledge; theory of mind; experimental semiotics
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.1414886111

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. 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.