Categorizing human vocal signals depends on an integrated auditory‐frontal cortical network

Abstract

Voice signals are relevant for auditory communication and suggested to be processed in dedicated auditory cortex (AC) regions. While recent reports highlighted an additional role of the inferior frontal cortex (IFC), a detailed description of the integrated functioning of the AC–IFC network and its task relevance for voice processing is missing. Using neuroimaging, we tested sound categorization while human participants either focused on the higher‐order vocal‐sound dimension (voice task) or feature‐based intensity dimension (loudness task) while listening to the same sound material. We found differential involvements of the AC and IFC depending on the task performed and whether the voice dimension was of task relevance or not. First, when comparing neural vocal‐sound processing of our task‐based with previously reported passive listening designs we observed highly similar cortical activations in the AC and IFC. Second, during task‐based vocal‐sound processing we observed voice‐sensitive responses in the AC and IFC whereas intensity processing was restricted to distinct AC regions. Third, the IFC flexibly adapted to the vocal‐sounds' task relevance, being only active when the voice dimension was task relevant. Forth and finally, connectivity modeling revealed that vocal signals independent of their task relevance provided significant input to bilateral AC. However, only when attention was on the voice dimension, we found significant modulations of auditory‐frontal connections. Our findings suggest an integrated auditory‐frontal network to be essential for behaviorally relevant vocal‐sounds processing. The IFC seems to be an important hub of the extended voice network when representing higher‐order vocal objects and guiding goal‐directed behavior.

Effective connectivity underlying reward‐based executive control

“…This individualized peak approach allows targeting those regions on the single‐subject level that are most likely to drive ongoing neural processes in the group level while ensuring that individual regions remain comparable. The approach is in line with prior comparable studies examining task‐related DCM effects (Heim et al, 2009; Kleineberg et al, 2018; Roswandowitz, Swanborough, & Frühholz, 2021).…”

Disrupting inferior frontal cortex activity alters affect decoding efficiency from clear but not from ambiguous affective speech

“…For the affective forced choice task, we created blends of vocally expressed anger and fear using a voice morphing procedure (1, 2) on a set of commonly available and validated vocal affective bursts, namely the Montreal affective voice database or 'MAV' (3). From this database we selected five male and five female voices.…”

“…Unlike clear affective expressions in voices which represent categorical certainty as predicted by the second hypothesis, ambiguous vocal affect might trigger computations in the IFC given their challenging perceptual and cognitive processing according to the first hypothesis. Both cases might additionally require integrated IFC-STC functioning in terms of neural connectivity (Roswandowitz, Swanborough et al 2020), either for top-down IFC-to-STC facilitations or as co-representations of categorical affective information (Steiner, Bobin et al 2021). The use of transcranial magnetic stimulation (TMS) appears to be a reliable and non-invasive option to especially inhibit a proper functioning of computations performed in the IFC in this context.…”

“…The neural processing and classification of acoustic information involves a cortical neural network beyond auditory decoding in the auditory cortex (AC; Staib and Frühholz 2020). The core of this neural network especially for decoding acoustic and social information conveyed by acoustic voice signals involves an integrated functioning of the AC together with various regions in the inferior frontal cortex (IFC; Rauschecker and Scott 2009, Roswandowitz, Swanborough et al 2020). This auditory-frontal network is especially relevant for extracting socio-affective information from voice signals (Frühholz and Grandjean 2012, Frühholz and Grandjean 2013, Dricu, Ceravolo et al 2017, Swanborough, Staib et al 2020), such as decoding emotional information expressed in affective voices and affective intonations in speech.…”

“…Within this broad auditory-frontal-limbic network for voice signals processing and voice information decoding (Dricu, Ceravolo et al 2017, Dricu and Frühholz 2020, Frühholz and Schweinberger 2020), the involvement of the IFC in decoding emotions from affective speech has been consistently reported (Frühholz and Schweinberger 2020, Roswandowitz, Swanborough et al 2020, Swanborough, Staib et al 2020), but its functional role in the neural network and its functional contribution to voice signal processing and especially in vocal affect decoding remained debated. Some previous studies indicated that social affective decoding from voice seemed restricted to the AC (Grandjean, Sander et al 2005, Ethofer, Van De Ville et al 2009) without any functional relevance of the IFC.…”