How does the brain mediate interpretation of incongruent auditory emotions? The neural response to prosody in the presence of conflicting lexico‐semantic cues

Abstract

We frequently encounter conflicting emotion cues. This study examined how the neural response to emotional prosody differed in the presence of congruent and incongruent lexico-semantic cues. Two hypotheses were assessed: (i) decoding emotional prosody with conflicting lexico-semantic cues would activate brain regions associated with cognitive conflict (anterior cingulate and dorsolateral prefrontal cortex) or (ii) the increased attentional load of incongruent cues would modulate the activity of regions that decode emotional prosody (right lateral temporal cortex). While the participants indicated the emotion conveyed by prosody, functional magnetic resonance imaging data were acquired on a 3T scanner using blood oxygenation level-dependent contrast. Using SPM5, the response to congruent cues was contrasted with that to emotional prosody alone, as was the response to incongruent lexico-semantic cues (for the 'cognitive conflict' hypothesis). The right lateral temporal lobe region of interest analyses examined modulation of activity in this brain region between these two contrasts (for the 'prosody cortex' hypothesis). Dorsolateral prefrontal and anterior cingulate cortex activity was not observed, and neither was attentional modulation of activity in right lateral temporal cortex activity. However, decoding emotional prosody with incongruent lexico-semantic cues was strongly associated with left inferior frontal gyrus activity. This specialist form of conflict is therefore not processed by the brain using the same neural resources as non-affective cognitive conflict and neither can it be handled by associated sensory cortex alone. The recruitment of inferior frontal cortex may indicate increased semantic processing demands but other contributory functions of this region should be explored.

Processing of emotional vocalizations in bilateral inferior frontal cortex

“…Recent neuroimaging studies found several right IFC peak activations distributed from the posterior to the anterior IFC located in BA 44 Kotz et al, 2003), BA 45 (Bach et al, 2008;Beaucousin et al, 2007;Ethofer et al, 2006;Sander et al, 2005), and BA 47 (Bach et al, 2008;Beaucousin et al, 2007;Belin et al, 2008a;Ethofer et al, 2009;Mitchell, 2006;Sander et al, 2005), as well as in the fOP Kotz et al, 2003;Mitchell et al, 2003;Schirmer et al, 2004) (see Fig. 2).…”

“…The IFC is primarily assumed to explicitly and cognitively evaluate the emotional value of voices (Ethofer et al, 2012;Leitman et al, 2010), such as occurs in the evaluation, labeling, or categorization of vocal expressions. This conclusion arises from the fact that studies usually find IFC activity when participants are asked to attentively and explicitly focus on the emotional value of voices (Beaucousin et al, 2007;Ethofer et al, 2006;Mitchell, 2006;Wildgruber et al, 2002), or when the decoding becomes more challenging because of ambiguous acoustic cues (Leitman et al, 2010;Schirmer et al, 2004) or conflicting emotional cues (Leitman et al, 2010;Schirmer et al, 2004). Both conditions, the attentive and explicit task, as well the conditions of more challenging decoding, represent first-order executive processes.…”

“…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).…”

“…However, it seems that the medium of vocal expressions as a bottom-up factor can also influence this peak distribution. Concerning this medium or nature of vocalizations, vocal expressions of emotions can be purely nonverbal, such as laughs, cries, or screams (Sauter et al, 2010;Simon-Thomas et al, 2009), but they can also be superimposed on semantically neutral Kotz et al, 2003;Leitman et al, 2010) and semantically emotional language (Beaucousin et al, 2007;Mitchell, 2006;Mitchell et al, 2003;Schirmer et al, 2004), as well as on pseudospeech (Bach et al, 2008;Sander et al, 2005). Given this distinction between nonverbal vocal expressions and emotional prosody, it might be assumed that emotional intonations superimposed on speech strongly engage the left IFC, whereas nonverbal expressions activate the right IFC (Meyer 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).…”