Time Course of the Involvement of the Right Anterior Superior Temporal Gyrus and the Right Fronto-Parietal Operculum in Emotional Prosody Perception Marjolijn Hoekert1*, Leonie Bais1, Rene´ S. Kahn 2 , Andre´ Aleman1 1 BCN Neuroimaging Center, University of Groningen, Groningen, The Netherlands, 2 Department of Psychiatry, University Medical Center Utrecht, Utrecht, The Netherlands Abstract In verbal communication, not only the meaning of the words convey information, but also the tone of voice (prosody) conveys crucial information about the emotional state and intentions of others. In various studies right frontal and right temporal regions have been found to play a role in emotional prosody perception. Here, we used triple-pulse repetitive transcranial magnetic stimulation (rTMS) to shed light on the precise time course of involvement of the right anterior superior temporal gyrus and the right fronto-parietal operculum. We hypothesized that information would be processed in the right anterior superior temporal gyrus before being processed in the right fronto-parietal operculum. Right-handed healthy subjects performed an emotional prosody task. During listening to each sentence a triplet of TMS pulses was applied to one of the regions at one of six time points (400–1900 ms). Results showed a significant main effect of Time for right anterior superior temporal gyrus and right fronto-parietal operculum. The largest interference was observed half-way through the sentence. This effect was stronger for withdrawal emotions than for the approach emotion. A further experiment with the inclusion of an active control condition, TMS over the EEG site POz (midline parietal-occipital junction), revealed stronger effects at the fronto-parietal operculum and anterior superior temporal gyrus relative to the active control condition. No evidence was found for sequential processing of emotional prosodic information from right anterior superior temporal gyrus to the right fronto-parietal operculum, but the results revealed more parallel processing. Our results suggest that both right fronto-parietal operculum and right anterior superior temporal gyrus are critical for emotional prosody perception at a relatively late time period after sentence onset. This may reflect that emotional cues can still be ambiguous at the beginning of sentences, but become more apparent half-way through the sentence. Citation: Hoekert M, Bais L, Kahn RS, Aleman A (2008) Time Course of the Involvement of the Right Anterior Superior Temporal Gyrus and the Right Fronto- Parietal Operculum in Emotional Prosody Perception. PLoS ONE 3(5): e2244. doi:10.1371/journal.pone.0002244 Editor: Ernest Greene, University of Southern California, United States of America Received February 25, 2008; Accepted April 10, 2008; Published May 21, 2008 Copyright: 2008 Hoekert et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: M.H. was supported by a research grant from the Netherlands organization for Scientific Research (400 04333). A.A. was also supported by a grant from the Netherlands organization for Scientific Research (016.026.027). This organization did not have any influence on the design and the conduct of the study. Competing Interests: The authors have declared that no competing interests exist. * E-mail: L.m.hoekert@med.umcg.nl Introduction Besides the semantic meaning of words, features such as intonation, loudness and accents in speech may convey crucial information about the emotional state of the speaker. The term emotional prosody describes these non-linguistic cues in spoken language. The ability to perceive emotional prosody is crucial for understanding someone’s true communicative intent and thereby for adequate social functioning [1]. Emotional prosody depends on intact functioning of the right hemisphere, although some studies suggest that it may also involve left hemisphere regions [2–7]. Imaging and patient studies have yielded discrepant data with respect to lateralization and location of brain regions contributing to the process of emotional prosody perception. Most of these studies show right (inferior or orbital) frontal [3,6–13] and right temporal regions [5,7–9,11,12,14–21]. Others show bilateral frontal [2–7,21], left temporal [3,8] and right inferior parietal lobule [4,13] involvement. To further delineate the network of emotional prosody recognition, in the present experiment both a frontal and temporal location were targeted with transcranial magnetic stimulation (TMS). In TMS, brief magnetic pulses are delivered that penetrate the skull and disrupt neural processing in a non-invasive, reversible way [22]. Exact TMS sites for the present study were based on imaging studies that used sentences as stimuli and on a recent TMS study [23]. In the latter study increased reaction times were observed after modulation of the right fronto-parietal operculum [23]. This was a specific effect, only observed for a condition requiring emotional prosody discrimination, and not for a condition that required discriminating emotional semantics. Involvement of the right fronto-parietal operculum in the perception of emotional prosody was also found in other studies [3,5,7,21]. The right fronto-parietal operculum forms part of the secondary somatosensory cortex. It has been suggested that knowledge about emotions expressed by other people might rely on a situation of body states associated with that emotion in the perceiver [24]. According to this theory, explicit recognition of an affective state in others depends on recruitment of one’s own somatic expression representation associated with such emotion [24]. Activation of the somatosensory representation allows the observer to simulate the perceived emotion and evaluate and ‘feel’ it. The involvement of PLoS ONE | www.plosone.org 1 May 2008 | Volume 3 | Issue 5 | e2244