Emotion processing in words: a test of the neural re-use hypothesis using surface and intracranial EEG

Abstract

This study investigates the spatiotemporal brain dynamics of emotional information processing during reading using a combination of surface and intracranial electroencephalography (EEG). Two different theoretical views were opposed. According to the standard psycholinguistic perspective, emotional responses to words are generated within the reading network itself subsequent to semantic activation. According to the neural re-use perspective, brain regions that are involved in processing emotional information contained in other stimuli (faces, pictures, smells) might be in charge of the processing of emotional information in words as well. We focused on a specific emotion-disgust-which has a clear locus in the brain, the anterior insula. Surface EEG showed differences between disgust and neutral words as early as 200 ms. Source localization suggested a cortical generator of the emotion effect in the left anterior insula. These findings were corroborated through the intracranial recordings of two epileptic patients with depth electrodes in insular and orbitofrontal areas. Both electrodes showed effects of disgust in reading as early as 200 ms. The early emotion effect in a brain region (insula) that responds to specific emotions in a variety of situations and stimuli clearly challenges classic sequential theories of reading in favor of the neural re-use perspective.

Keywords: ERP; disgust; emotion; reading; word recognition.

Fig. 1

Time-course model of visual word recognition proposed by Grainger and Holcomb (, Figure 12).

Fig. 2

Schematic view of the scalp electrode montage used for the analysis.

Fig. 3

(A) ERPs (mean amplitudes in µV) to the NoGo trials for disgust and neutral word categories at POz. Right, topography of ERPs at the averaged time window of the EPN latency, (B) ERPs (mean amplitudes in µV) to the NoGo trials for the disgust and neutral word categories at FCz. Right, topography of ERPs at the averaged time window of the N400 latency.

Fig. 4

sLORETA maps for the N400 component for the contrast between Disgust and Neutral (NoGo) words, centered on the maximum peak activity, in the left insula.

Fig. 5

Intracranial recordings. Left panel: Anatomical MRIs showing the recording site. R: right hemisphere; L: left hemisphere. On the right panel: Time course of the intracranial potentials in response to disgust (plain line) and neutral (dotted line) words.