Bidirectional Connectivity Between Broca's Area and Wernicke's Area During Interactive Verbal Communication

Abstract

Aim: This investigation aims to advance the understanding of neural dynamics that underlies live and natural interactions during spoken dialogue between two individuals. Introduction: The underlying hypothesis is that functional connectivity between canonical speech areas in the human brain will be modulated by social interaction. Methods: Granger causality was applied to compare directional connectivity across Broca's and Wernicke's areas during verbal conditions consisting of interactive and noninteractive communication. Thirty-three pairs of healthy adult participants alternately talked and listened to each other while performing an object naming and description task that was either interactive or not during hyperscanning with functional near-infrared spectroscopy (fNIRS). In the noninteractive condition, the speaker named and described a picture-object without reference to the partner's description. In the interactive condition, the speaker performed the same task but included an interactive response about the preceding comments of the partner. Causality measures of hemodynamic responses from Broca's and Wernicke's areas were compared between real, surrogate, and shuffled trials within dyads. Results: The interactive communication was characterized by bidirectional connectivity between Wernicke's and Broca's areas of the listener's brain. Whereas this connectivity was unidirectional in the speaker's brain. In the case of the noninteractive condition, both speaker's and listener's brains showed unidirectional top-down (Broca's area to Wernicke's area) connectivity. Conclusion: Together, directional connectivity as determined by Granger analysis reveals bidirectional flow of neuronal information during dynamic two-person verbal interaction for processes that are active during listening (reception) and not during talking (production). Findings are consistent with prior contrast findings (general linear model) showing neural modulation of the receptive language system associated with Wernicke's area during a two-person live interaction. Impact statement The neural dynamics that underlies real-life social interactions is an emergent topic of interest. Dynamically coupled cross-brain neural mechanisms between interacting partners during verbal dialogue have been shown within Wernicke's area. However, it is not known how within-brain long-range neural mechanisms operate during these live social functions. Using Granger causality analysis, we show bidirectional neural activity between Broca's and Wernicke's areas during interactive dialogue compared with a noninteractive control task showing only unidirectional activity. Findings are consistent with an Interactive Brain Model where long-range neural mechanisms process interactive processes associated with rapid and spontaneous spoken social cues.

Keywords: Granger causality; effective connectivity; functional near-infrared spectroscopy; human language interactions; hyperscanning; two-person neuroscience; verbal dialogue.

FIG. 1.

fNIRS channel layout. Forty-two fNIRS channels were assigned with each participant over both hemispheres of the scalp. Channel distances were based on cap size to fit the head of the subject, and the channel separations were either 2.75 cm for small heads or 3.0 cm for large heads (Dravida et al., 2017). The optode positions were digitized from each participant and the average channel positions of all participants were projected onto the normalized brain image. fNIRS, functional near-infrared spectroscopy.

FIG. 2.

Diagram of experimental design (a) including original (b) and shuffled (c, d) fNIRS signals for GC analysis. Dyads of participants performed an object naming and description task alternately. Background colors of gray, green, and yellow indicate corresponding epochs. The Granger causality was calculated with original and shuffled data. GC, Granger causality.

FIG. 3.

Simulation summary investigating detectability of Granger causal relationship with fNIRS data. (a) Causal relationship was assumed between two ROIs in each of two brains. (b) Example of simulated fNIRS signals. Signals at the receiver ROIs (gray lines in x₂ and x₄) were assumed to have neuronal delay from those at the sender ROIs (x₁ and x₃) for information transmission. The signals at the receiver ROIs were further shifted back to opposing direction of the neuronal delay (black lines in x₂ and x₄) to simulate the worst-case scenario leading to the underestimation of causal relationship. Gaussian noise was further added to these simulated signals for the GC analysis. (c) Heat maps showing the ratio of correctly (blue panels) or incorrectly (orange panels) detected Granger causal relationship with varied sampling Fs of the data. The number in each cell indicates the percentage of detecting valid GC among 100 trials of simulation. At the sampling rate of the original fNIRS GC analysis (Fs = 3.7 Hz), the assumed directional connectivity was perfectly detected, while the false detection was scarce. (d) Changes of mean detection rates for true and false connectivity with different sampling frequencies. The mean detection rates were calculated as the average occurrence ratio of valid GC over true (from x₁ to x₂ and from x₃ to x₄: filled circles) or false (the other pairs of ROIs: open triangles) combinations of signals. Fs, frequencies; ROIs, regions of interest.

FIG. 4.

GLM contrast map of deOxyHb signals between talking and listening tasks in dialogue condition. Red/yellow indicates regions with larger activity in talking relative to listening, and blue/cyan indicates those with larger activity in listening relative to talking. Please also refer to Table 1 for detailed anatomical locations of the activities. deOxyHb, deoxyhemoglobin; GLM, general linear model.

FIG. 5.

Schematic representation of Granger causal connectivity between canonical speech areas during two-person dialogue with interaction (a, b) and monologue talking and listening (c, d). The directional connectivity that showed statistical inference over both surrogate and shuffled controls was illustrated in the figure. For the speaking task (b, d), the observed direction of connectivity is from Broca's area to Wernicke's area regardless of existence or inexistence of interaction. However, for the listening task, the connectivity is bidirectional including both bottom-up and top-down directions under interaction (a), whereas it is unilateral without interaction (c). The nodes were visualized with the BrainNet Viewer (Xia et al., 2013).