Emotional speech synchronizes brains across listeners and engages large-scale dynamic brain networks

Abstract

Speech provides a powerful means for sharing emotions. Here we implement novel intersubject phase synchronization and whole-brain dynamic connectivity measures to show that networks of brain areas become synchronized across participants who are listening to emotional episodes in spoken narratives. Twenty participants' hemodynamic brain activity was measured with functional magnetic resonance imaging (fMRI) while they listened to 45-s narratives describing unpleasant, neutral, and pleasant events spoken in neutral voice. After scanning, participants listened to the narratives again and rated continuously their feelings of pleasantness–unpleasantness (valence) and of arousal–calmness. Instantaneous intersubject phase synchronization (ISPS) measures were computed to derive both multi-subject voxel-wise similarity measures of hemodynamic activity and inter-area functional dynamic connectivity (seed-based phase synchronization, SBPS). Valence and arousal time series were subsequently used to predict the ISPS and SBPS time series. High arousal was associated with increased ISPS in the auditory cortices and in Broca's area, and negative valence was associated with enhanced ISPS in the thalamus, anterior cingulate, lateral prefrontal, and orbitofrontal cortices. Negative valence affected functional connectivity of fronto-parietal, limbic (insula, cingulum) and fronto-opercular circuitries, and positive arousal affected the connectivity of the striatum, amygdala, thalamus, cerebellum, and dorsal frontal cortex. Positive valence and negative arousal had markedly smaller effects. We propose that high arousal synchronizes the listeners' sound-processing and speech-comprehension networks, whereas negative valence synchronizes circuitries supporting emotional and self-referential processing.

Neural mechanisms for integrating consecutive and interleaved natural events

“…Scenes showing highest differences in ISC timecourses also contained moments of high suspense. In the GLM analysis, suspense was associated with activity in corticolimbic areas whose ISC and BOLD‐GLM responses are modulated by affective arousal [Nummenmaa et al, ], which is an important component of suspense experience [Lehne and Koelsch, ]. However, due to the slowness of the signals, the parametric test was very liberal.…”

Brain processes in women and men in response to emotive sounds

“…In general, auditory perception tasks deactivate the DMN (Abbott, Kim, Sponheim, Bustillo, & Calhoun, 2010; Binder et al, 1999; McKiernan et al, 2003). However, it has been reported that several factors influence the degree of the deactivation in this network, including the load of the task, the discriminability and presentation rate of stimuli, and the emotive valence and salience of the stimuli (Antrobus, 1968; Antrobus, Singer, & Greenberg, 1966; Binder et al, 1999; Giambra 1995; McGuire et al, 1996; McKiernan, Kaufman, Kucera-Thompson, & Binder, 2003; Nummenmaa et al, 2014; Pope & Singer, 1976; Shulman et al, 1997; Teasdale, Proctor, Lloyd, & Baddeley, 1993). In our study, infant crying exerted more interference than other sounds in women, capturing attentional resources from the SOT, and deactivation of the PCC reflected the disengagement from the task.…”

“…The observed weak deactivations in men might reflect a resource competition to process female adult crying and simultaneously count syllables. In fact, the DMN is partially activated in response to exogenous stimuli that have self-relevance (Li, Mai, & Liu, 2014; Nummenmaa et al, 2014; Vessel, Starr, & Rubin, 2013). The DMN is also positively activated when individuals evaluate their own (and others’) beliefs, perspectives, and mental states (Li et al, 2014).…”

“…In the GOT in the present study, the weak deactivation in men in association with female adult crying might indicate that this specific sound, more than the other sounds, elicits self-relevant processes which can contribute to mentally understanding others. Consequently, self-relevant processes, associated with the partial activation of the DMN, elicited by female adult crying, might explain the reduced deactivation of the MPFC and PCC in men in the GOT (Li et al, 2014; Nummenmaa et al, 2014). …”

Inter-subject phase synchronization differentiates neural networks underlying physical pain empathy

“…To examine the relationship between the synchronization time series resulting from the ICA with each task condition we used the convolved block regressors of the GLM as reference functions. As noted by others (Nummenmaa et al, 2014), conventional double-gamma HRF convolved regressors attempt to model a late undershoot of the HRF, which would not presumably be present in the case of a voxel synchronization time course (which would exhibit no undershoot). Thus, to get the suitable reference functions, we computed another GLM model using the gamma HRF in FSL to account for HRF lag and width, without an undershoot.…”