Cerebral Processing of Voice Gender Studied Using a Continuous Carryover fMRI Design

Abstract

Normal listeners effortlessly determine a person's gender by voice, but the cerebral mechanisms underlying this ability remain unclear. Here, we demonstrate 2 stages of cerebral processing during voice gender categorization. Using voice morphing along with an adaptation-optimized functional magnetic resonance imaging design, we found that secondary auditory cortex including the anterior part of the temporal voice areas in the right hemisphere responded primarily to acoustical distance with the previously heard stimulus. In contrast, a network of bilateral regions involving inferior prefrontal and anterior and posterior cingulate cortex reflected perceived stimulus ambiguity. These findings suggest that voice gender recognition involves neuronal populations along the auditory ventral stream responsible for auditory feature extraction, functioning in pair with the prefrontal cortex in voice gender perception.

Hemispheric association and dissociation of voice and speech information processing in stroke

“…Humans easily recognize different voices, and this ability is of considerable social importance. Voice-selective areas have been demonstrated in the human brain (Belin, Zattorre, & Ahad, 2002;Belin, Zattorre, Lafaille, Ahad, & Pike, 2000), localized bilaterally along the upper bank (middle and anterior) of the Superior Temporal Sulcus (STS) (Alho et al, 2006;Belin, et al, 2002), and also in the inferior and orbitofrontal cortex (Charest, Pernet, Latinus, Crabbe, & Belin, 2012;Fecteau, Armony, Joanete, & Belin 2005) as well as surrounding insular cortex (Johnstone, van Reekum, Oakes, & Davidson, 2006;Rama et al, 2004). This neural selectivity for voice has also been established in other mammals, in particular primates (Johnstone et al, 2006;Rama et al, 2004) and more recently dogs (Andics, Gacsi, Farago, Kis, & Miklosi, 2014).…”

“…Based on functional MRI (Belin, et al, 2002(Belin, et al, , 2000Charest et al, 2012) and Transcranial Magnetic Stimulation (Bestelemeyer, et al, 2011) results observed in healthy volunteers, we hypothesized that patients with right fronto-temporal stroke will show a deficit in gender categorization but intact phonological performances. Our results using both a qualitative (classification of percentage of responses) and a quantitative (signal detection theory) approach confirmed this hypothesis.…”

“…On one hand, studies comparing attention to voice vs. speech found voice specific effects over the right STS (von Kriegstein, Eger, Kleinschmidt, & Giraud, 2003), and this effect has been related to speaker identity (Schall, Kiebel, Maess, & von Kriegstein, 2014). On the other hand, using a continuous carry over-over design allowing acoustic from perceived distances to be distinguished during gender categorization, Charest et al, (2012) showed that the STS processes gender (and thus identity as well) related acoustic information whilst the right IFG is involved in perceived gender related distances. In most studies, stimuli are pitch equalized.…”

“…The ROI classification was performed by an expert neuro-radiologist (AF) with 12 years of experience, and following a detailed protocol 1 adapted from the International Stroke Trial III (Whiteley et al, 2006). Regions of Interest (ROI) considered were the middle/inferior frontal gyrus (involved in gender categorization (Fecteau, et al, 2005, Charest et al, 2012, Heschl's gyrus (also called Transverse Temporal gyrus -involved in language learning and spectral/pitch information processing (Warrier et al, 2009), the superior temporal gyrus (anterior/posterior, involved in general auditory processes but also voice perception, Belin, et al, 2004), the insula (involved in central auditory functions, in particular temporal resolution and sequencing (Bamiou et al, 2006) and the amygdala-hippocampal complex (involved in memory and emotional voice perception (Johnstone et al, 2006;Rama et al, 2004).…”

“…Stimuli were the same in both tasks, and participants had therefore to discard talker specific or phoneme specific information depending on the task at M A N U S C R I P T A C C E P T E D ACCEPTED MANUSCRIPT 3 hand. Given the importance of the right STS (Bestelemeyer, Belin, P., & Grosbras, 2011) and right Middle and Inferior Frontal Gyrus (MFG-IFG) (Charest et al, 2012) in talker information processing, we hypothesized that right hemisphere patients will show a dissociation between the two tasks. In contrast, following our hypothesis of co-optation of voice selective neurons in phoneme processing, we hypothesized that left hemispheric aphasic patients will not show such dissociation, while non-aphasic patient could be impaired for voice but not phoneme.…”