Distinct Frontal Regions Subserve Evaluation of Linguistic and Emotional Aspects of Speech Intonation

Abstract

In addition to the propositional content of verbal utterances, significant linguistic and emotional information is conveyed by the tone of speech. To differentiate brain regions subserving processing of linguistic and affective aspects of intonation, discrimination of sentences differing in linguistic accentuation and emotional expressiveness was evaluated by functional magnetic resonance imaging. Both tasks yielded rightward lateralization of hemodynamic responses at the level of the dorsolateral frontal cortex as well as bilateral thalamic and temporal activation. Processing of linguistic and affective intonation, thus, seems to be supported by overlapping neural networks comprising partially right-sided brain regions. Comparison of hemodynamic activation during the two different tasks, however, revealed bilateral orbito-frontal responses restricted to the affective condition as opposed to activation of the left lateral inferior frontal gyrus confined to evaluation of linguistic intonation. These findings indicate that distinct frontal regions contribute to higher level processing of intonational information depending on its communicational function. In line with other components of language processing, discrimination of linguistic accentuation seems to be lateralized to the left inferior-lateral frontal region whereas bilateral orbito-frontal areas subserve evaluation of emotional expressiveness.

Processing of emotional vocalizations in bilateral inferior frontal cortex

“…Similarly, emotional prosody, that is, the emotionally influenced tone of a voice (Banse and Scherer, 1996), elicits strong and replicable right IFC activation (e.g. Buchanan et al, 2000;George et al, 1996;Wildgruber et al, 2004). This finding supports early proposals of the critical involvement of the right hemisphere in prosody processing in general (Ross, 1981) and specifically emotional prosody (Ross andMonnot, 2008, 2011;Ross et al, 1997;van Lancker, 1980).…”

“…The left IFC thus might also decode emotional cues from nonspeech vocalizations, indicating that left IFC activity is not exclusive to syntacto-semantic speech processing, but serves more general functions during the processing of human utterances. Finally, although the IFC has been proposed to be involved in the explicit decoding of emotional prosody when attention is directed to the emotional cues in voices, IFC activity has also been found when attention is directed away from emotional cues in voices (Belin et al, 2008a;Fecteau et al, 2005;Morris et al, 1999;Wildgruber et al, 2004Wildgruber et al, , 2005 or during passive listening (Mitchell et al, 2003). This contradicts some proposals that the IFC is predominantly involved in the explicit evaluation of emotional voices or when attention is directly focused on the emotional value of voices (Bruck et al, 2011;Schirmer and Kotz, 2006;Wildgruber et al, 2009).…”

“…The available data support the notion of a cognitive controlled evaluation. But this seems not to be restricted to an explicit attentive focus on the emotional cues in voices, given that IFC activity was also found when the emotional value of voices was processed preattentively, such as when it was presented outside the focus of attention (Belin et al, 2008a;Buchanan et al, 2000;Fecteau et al, 2005;Morris et al, 1999;Sander et al, 2005;Wildgruber et al, 2004Wildgruber et al, , 2005.…”

“…Left hemispheric and particularly left IFC lesions result in impairments during the processing of emotional vocalizations (Pell, 1998), though right hemisphere lesions still show a more pervasive insensitivity to emotional prosody (Pell, 2006). However, it has been suggested that the left compared with the right IFC has only a supplementary processing role, such as prosody-related working memory processes Wildgruber et al, 2005), linguistic processing (Buchanan et al, 2000;Wildgruber et al, 2004), retrieval of semantic knowledge (Beaucousin et al, 2007), or semantic processing during impaired prosody processing (Mitchell, 2006;Schirmer and Kotz, 2006;Schirmer et al, 2004). Nonetheless, even when controlling for all secondary and language-related task effects, emotional vocalizations still elicit activity in the left IFC Kotz et al, 2003;Leitman et al, 2010;Sander et al, 2005).…”

“…First, many recent studies found bilateral (Beaucousin et al, 2007;Ethofer et al, 2006;Kotz et al, 2003;Morris et al, 1999) or even specific left IFC activity (Bach et al, 2008;Fecteau et al, 2005;Mitchell, 2006;Wildgruber et al, 2004) in response to emotional prosody in several subregions of the IFC (see Fig. 2).…”