Who is that? Brain networks and mechanisms for identifying individuals

Social animals can identify conspecifics by many forms of sensory input. However, whether the neuronal computations that support this ability to identify individuals rely on modality-independent convergence or involve ongoing synergistic interactions along the multiple sensory streams remains controversial. Direct neuronal measurements at relevant brain sites could address such questions, but this requires better bridging the work in humans and animal models. Here, we overview recent studies in nonhuman primates on voice and face identity-sensitive pathways and evaluate the correspondences to relevant findings in humans. This synthesis provides insights into converging sensory streams in the primate anterior temporal lobe (ATL) for identity processing. Furthermore, we advance a model and suggest how alternative neuronal mechanisms could be tested

People-selectivity, audiovisual integration and heteromodality in the superior temporal sulcus

The functional role of the superior temporal sulcus (STS) has been implicated in a number of studies, including those investigating face perception, voice perception, and face–voice integration. However, the nature of the STS preference for these ‘social stimuli’ remains unclear, as does the location within the STS for specific types of information processing. The aim of this study was to directly examine properties of the STS in terms of selective response to social stimuli. We used functional magnetic resonance imaging (fMRI) to scan participants whilst they were presented with auditory, visual, or audiovisual stimuli of people or objects, with the intention of localising areas preferring both faces and voices (i.e., ‘people-selective’ regions) and audiovisual regions designed to specifically integrate person-related information. Results highlighted a ‘people-selective, heteromodal’ region in the trunk of the right STS which was activated by both faces and voices, and a restricted portion of the right posterior STS (pSTS) with an integrative preference for information from people, as compared to objects. These results point towards the dedicated role of the STS as a ‘social-information processing’ centre

Cerebral correlates and statistical criteria of cross-modal face and voice integration

Perception of faces and voices plays a prominent role in human social interaction, making multisensory integration of cross-modal speech a topic of great interest in cognitive neuroscience. How to define po- tential sites of multisensory integration using functional magnetic resonance imaging (fMRI) is currently under debate, with three statistical criteria frequently used (e.g., super-additive, max and mean criteria). In the present fMRI study, 20 participants were scanned in a block design under three stimulus conditions: dynamic unimodal face, unimodal voice and bimodal face–voice. Using this single dataset, we examine all these statistical criteria in an attempt to define loci of face–voice integration. While the super-additive and mean criteria essentially revealed regions in which one of the unimodal responses was a deactivation, the max criterion appeared stringent and only highlighted the left hippocampus as a potential site of face– voice integration. Psychophysiological interaction analysis showed that connectivity between occipital and temporal cortices increased during bimodal compared to unimodal conditions. We concluded that, when investigating multisensory integration with fMRI, all these criteria should be used in conjunction with ma- nipulation of stimulus signal-to-noise ratio and/or cross-modal congruency

Investigating the Neural Basis of Audiovisual Speech Perception with Intracranial Recordings in Humans

Speech is inherently multisensory, containing auditory information from the voice and visual information from the mouth movements of the talker. Hearing the voice is usually sufficient to understand speech, however in noisy environments or when audition is impaired due to aging or disabilities, seeing mouth movements greatly improves speech perception. Although behavioral studies have well established this perceptual benefit, it is still not clear how the brain processes visual information from mouth movements to improve speech perception. To clarify this issue, I studied the neural activity recorded from the brain surfaces of human subjects using intracranial electrodes, a technique known as electrocorticography (ECoG). First, I studied responses to noisy speech in the auditory cortex, specifically in the superior temporal gyrus (STG). Previous studies identified the anterior parts of the STG as unisensory, responding only to auditory stimulus. On the other hand, posterior parts of the STG are known to be multisensory, responding to both auditory and visual stimuli, which makes it a key region for audiovisual speech perception. I examined how these different parts of the STG respond to clear versus noisy speech. I found that noisy speech decreased the amplitude and increased the across-trial variability of the response in the anterior STG. However, possibly due to its multisensory composition, posterior STG was not as sensitive to auditory noise as the anterior STG and responded similarly to clear and noisy speech. I also found that these two response patterns in the STG were separated by a sharp boundary demarcated by the posterior-most portion of the Heschl’s gyrus. Second, I studied responses to silent speech in the visual cortex. Previous studies demonstrated that visual cortex shows response enhancement when the auditory component of speech is noisy or absent, however it was not clear which regions of the visual cortex specifically show this response enhancement and whether this response enhancement is a result of top-down modulation from a higher region. To test this, I first mapped the receptive fields of different regions in the visual cortex and then measured their responses to visual (silent) and audiovisual speech stimuli. I found that visual regions that have central receptive fields show greater response enhancement to visual speech, possibly because these regions receive more visual information from mouth movements. I found similar response enhancement to visual speech in frontal cortex, specifically in the inferior frontal gyrus, premotor and dorsolateral prefrontal cortices, which have been implicated in speech reading in previous studies. I showed that these frontal regions display strong functional connectivity with visual regions that have central receptive fields during speech perception

Short review A "voice patch" system in the primate brain for processing vocal information?

International audienceWe review behavioural and neural evidence for the processing of information contained in conspecific vocalizations (CVs) in three primate species: humans, macaques and marmosets. We focus on abilities that are present and ecologically relevant in all three species: the detection and sensitivity to CVs; and the processing of identity cues in CVs. Current evidence, although fragmentary, supports the notion of a "voice patch system" in the primate brain analogous to the face patch system of visual cortex: a series of discrete, interconnected cortical areas supporting increasingly abstract representations of the vocal input. A central question concerns the degree to which the voice patch system is conserved in evolution. We outline challenges that arise and suggesting potential avenues for comparing the organization of the voice patch system across primate brains

Investigating the Neural Correlates of Voice versus Speech-Sound Directed Information in Pre-School Children

Studies in sleeping newborns and infants propose that the superior temporal sulcus is involved in speech processing soon after birth. Speech processing also implicitly requires the analysis of the human voice, which conveys both linguistic and extra-linguistic information. However, due to technical and practical challenges when neuroimaging young children, evidence of neural correlates of speech and/or voice processing in toddlers and young children remains scarce. In the current study, we used functional magnetic resonance imaging (fMRI) in 20 typically developing preschool children (average age = 5.8 y; range 5.2–6.8 y) to investigate brain activation during judgments about vocal identity versus the initial speech sound of spoken object words. FMRI results reveal common brain regions responsible for voice-specific and speech-sound specific processing of spoken object words including bilateral primary and secondary language areas of the brain. Contrasting voice-specific with speech-sound specific processing predominantly activates the anterior part of the right-hemispheric superior temporal sulcus. Furthermore, the right STS is functionally correlated with left-hemispheric temporal and right-hemispheric prefrontal regions. This finding underlines the importance of the right superior temporal sulcus as a temporal voice area and indicates that this brain region is specialized, and functions similarly to adults by the age of five. We thus extend previous knowledge of voice-specific regions and their functional connections to the young brain which may further our understanding of the neuronal mechanism of speech-specific processing in children with developmental disorders, such as autism or specific language impairments

Functional connectivity within the voice perception network and its behavioural relevance

International audienceRecognizing who is speaking is a cognitive ability characterized by considerable individual differences, which could relate to the inter-individual variability observed in voice-elicited BOLD activity. Since voice perception is sustained by a complex brain network involving temporal voice areas (TVAs) and, even if less consistently, extra-temporal regions such as frontal cortices, functional connectivity (FC) during an fMRI voice localizer (passive listening of voices vs non-voices) has been computed within twelve temporal and frontal voice-sensitive regions ("voice patches") individually defined for each subject (N ¼ 90) to account for inter-individual variability. Results revealed that voice patches were positively co-activated during voice listening and that they were characterized by different FC pattern depending on the location (anterior/posterior) and the hemisphere. Importantly, FC between right frontal and temporal voice patches was behaviorally relevant: FC significantly increased with voice recognition abilities as measured in a voice recognition test performed outside the scanner. Hence, this study highlights the importance of frontal regions in voice perception and it supports the idea that looking at FC between stimulus-specific and higher-order frontal regions can help understanding individual differences in processing social stimuli such as voices

Neural mechanisms for voice recognition

We investigated neural mechanisms that support voice recognition in a training paradigm with fMRI. The same listeners were trained on different weeks to categorize the mid-regions of voice-morph continua as an individual's voice. Stimuli implicitly defined a voice-acoustics space, and training explicitly defined a voice-identity space. The predefined centre of the voice category was shifted from the acoustic centre each week in opposite directions, so the same stimuli had different training histories on different tests. Cortical sensitivity to voice similarity appeared over different time-scales and at different representational stages. First, there were short-term adaptation effects: Increasing acoustic similarity to the directly preceding stimulus led to haemodynamic response reduction in the middle/posterior STS and in right ventrolateral prefrontal regions. Second, there were longer-term effects: Response reduction was found in the orbital/insular cortex for stimuli that were most versus least similar to the acoustic mean of all preceding stimuli, and, in the anterior temporal pole, the deep posterior STS and the amygdala, for stimuli that were most versus least similar to the trained voice-identity category mean. These findings are interpreted as effects of neural sharpening of long-term stored typical acoustic and category-internal values. The analyses also reveal anatomically separable voice representations: one in a voice-acoustics space and one in a voice-identity space. Voice-identity representations flexibly followed the trained identity shift, and listeners with a greater identity effect were more accurate at recognizing familiar voices. Voice recognition is thus supported by neural voice spaces that are organized around flexible ‘mean voice’ representations

SELECTIVE ASSOCIATIVE PHONAGNOSIA AFTER RIGHT ANTERIOR TEMPORAL STROKE

We report the case of a 48 year old men who developed a selective impairment in famous voice recognition after ischemic stroke in right subcortical structures (lenticular nucleus and head of the caudate) and right anterior temporal lobe. He underwent fibrinolytic treatment. During the following days he progressively recovered and was discharged without neurological focal sign. Patent foramen ovale was found. When he got back to his house he noticed that he was unable to recognize the voice of his favoured singers and needed to ask who was the singer to his relatives. Neuropsychological examination revealed a selective impairment in famous voice recognition in the absence of alteration of voice perception, face perception and famous face recognition. All other neuropsychological domains were spared. In particular language, memory and executive functions were intact. Neuroimaging carried out by means of PET and MRI revealed two small ischemic lesions in the right subcortical region, involving lenticular and caudate nuclei and in the right temporal pole. To our knowledge, this is the first case described in literature of a patient showing a selective associative phonagnosia after right anterior temporal stroke. The present case helps to clarify the brain circuits underlying famous voice recognition and adds evidence in favour of a right hemisphere involvement in processing knowledge of familiar voices. These findings are discussed in relation to current models of brain organization of person-specific and general semantic knowledge.

Specific Brain Networks during Explicit and Implicit Decoding of Emotional Prosody

To better define the underlying brain network for the decoding of emotional prosody, we recorded high-resolution brain scans during an implicit and explicit decoding task of angry and neutral prosody. Several subregions in the right superior temporal gyrus (STG) and bilateral in the inferior frontal gyrus (IFG) were sensitive to emotional prosody. Implicit processing of emotional prosody engaged regions in the posterior superior temporal gyrus (pSTG) and bilateral IFG subregions, whereas explicit processing relied more on mid STG, left IFG, amygdala, and subgenual anterior cingulate cortex. Furthermore, whereas some bilateral pSTG regions and the amygdala showed general sensitivity to prosody-specific acoustical features during implicit processing, activity in inferior frontal brain regions was insensitive to these features. Together, the data suggest a differentiated STG, IFG, and subcortical network of brain regions, which varies with the levels of processing and shows a higher specificity during explicit decoding of emotional prosod