Activation of Auditory Cortex by Anticipating and Hearing Emotional Sounds: An MEG Study

Koichi Yokosawa,Siina Pamilo,Lotta Hirvenkari,Elina Pihko,Riitta Hari

doi:10.1371/journal.pone.0080284

Abstract

To study how auditory cortical processing is affected by anticipating and hearing of long emotional sounds, we recorded auditory evoked magnetic fields with a whole-scalp MEG device from 15 healthy adults who were listening to emotional or neutral sounds. Pleasant, unpleasant, or neutral sounds, each lasting for 6 s, were played in a random order, preceded by 100-ms cue tones (0.5, 1, or 2 kHz) 2 s before the onset of the sound. The cue tones, indicating the valence of the upcoming emotional sounds, evoked typical transient N100m responses in the auditory cortex. During the rest of the anticipation period (until the beginning of the emotional sound), auditory cortices of both hemispheres generated slow shifts of the same polarity as N100m. During anticipation, the relative strengths of the auditory-cortex signals depended on the upcoming sound: towards the end of the anticipation period the activity became stronger when the subject was anticipating emotional rather than neutral sounds. During the actual emotional and neutral sounds, sustained fields were predominant in the left hemisphere for all sounds. The measured DC MEG signals during both anticipation and hearing of emotional sounds implied that following the cue that indicates the valence of the upcoming sound, the auditory-cortex activity is modulated by the upcoming sound category during the anticipation period.

Highlights

Humans detect positive and negative emotions from both linguistic and nonlinguistic utterances [1] as well as from environmental sounds, such as crashes, breaking of glass, and music
We measured cortical auditory-evoked magnetic fields to nonemotional cue tones and to the subsequent emotion-arousing and neutral sounds to assess the effect of emotional content of the sound on auditory-cortex activity, both during anticipation and hearing of the sounds
In line with earlier demonstration of auditory-cortex activation before an auditory imperative stimulus [23], the auditory cortices in both hemispheres were activated during the whole silent anticipation period, the activity became weaker towards the beginning of the emotional and neutral sounds

Summary

Introduction

Humans detect positive and negative emotions from both linguistic and nonlinguistic utterances [1] as well as from environmental sounds, such as crashes, breaking of glass, and music. Emotional pictures, compared with neutral pictures, can enhance the processing already in the early visual cortices [2]. The auditory cortices are affected by emotion. Cortices associated with auditory function—in addition to several cortical and subcortical areas commonly related to emotional processes—react more strongly to emotional than neutral prosody [3,4,5]. In addition to human voice, other types of complex emotional sounds lead to increased activation of the auditory cortices [10]. Even neutral tones conditioned in advance to emotional valence affect the auditorycortex 100-ms neuromagnetic response N100m [11]

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