Temporal voice areas exist in autism spectrum disorder but are dysfunctional for voice identity recognition

The ability to recognise the identity of others is a key requirement for successful communication. Brain regions that respond selectively to voices exist in humans from early infancy on [1]. Currently it is unclear whether dysfunction of these voice-sensitive regions can explain voice identity recognition impairments. Here, we used functional magnetic resonance imaging (fMRI) to investigate voice processing in a population that has been reported to have no voice-sensitive regions [2] and difficulties in voice identity recognition [3]: Autism spectrum disorder (ASD). Sixteen adults with high-functioning ASD and sixteen typically developing controls (matched pairwise on age, gender, and IQ) participated in two independent fMRI experiments. In the first fMRI experiment (vocal sound experiment), participants passively listened to blocks of vocal (speech and non-speech) and non-vocal sounds (e.g. musical instruments, nature, animals) [4]. In the second fMRI experiment (voice recognition experiment), participants performed voice identity recognition and speech recognition tasks on the same stimulus material [5]. On the behavioural level, the ASD group performed worse as compared to controls in the voice identity recognition task whereas both groups performed equally well in the speech recognition task. In the vocal sound experiment there was greater voice-sensitive blood-oxygenation-level-dependent [BOLD] response along the bilateral STS/STG when participants listened to vocal as compared to non-vocal sounds in the ASD and in the control group. In contrast, in the voice recognition experiment the ASD group showed reduced BOLD responses to the voice identity recognition in contrast to the speech recognition task compared to the control group in the right posterior STS/STG– a region that has been previously implicated in processing acoustic voice features and unfamiliar voices [5, 6]. The right anterior STS/STG correlated with voice identity recognition performance in controls but not in the ASD group. Our results refute the earlier report that individuals with ASD have no responses in voice-sensitive regions [2]. The findings suggest that right STS/STG dysfunction is critical for explaining voice recognition impairments in high-functioning ASD. We provide evidence that voice-sensitive regions in the brain play a critical role in the recognition of vocal identity, beyond their role in discriminating voices from non-vocal sounds. Furthermore, our results suggest that it is the posterior temporal lobe voice region that integrates the acoustic characteristics of the voice into a coherent percept. References [1] Grossmann, Oberecker, Koch, & Friederici (2010). The developmental origins of voice processing in the human brain. Neuron, 65(6), 852-858. [2] Gervais, Belin, Boddaert, Leboyer, Coez, . . . Zilbovicius (2004). Abnormal cortical voice processing in autism. NatureNeuroscience, 7(8), 801-802. [3] Schelinski, Riedel, & von Kriegstein (2014). Visual abilities are important for auditory-only speech recognition: evidence from autism spectrum disorder. Neuropsychologia, 65, 1-11. [4] Belin, Zatorre, Lafaille, Ahad, & Pike (2000). Voice-selective areas in human auditory cortex. Nature, 403(6767), 309-312. [5] von Kriegstein, & Giraud (2004). Distinct functional substrates along the right superior temporal sulcus for the processing of voices. Neuroimage, 22(2), 948-955. [6] Warren, Scott, Price, & Griffiths (2006). Human brain mechanisms for the early analysis of voices. Neuroimage, 31(3), 1389-1397