Voice Area Research Articles

Species-Specific, But Functionally Homologous Representation of Vocalizations in the Auditory Cortex of Humans and Macaques

How the evolution of speech has transformed the human auditory cortex compared to other primates remains unclear. Here we report a functional homology in the cerebral processing of vocalizations by macaques and humans, using comparative fMRI and a condition-rich auditory stimulation paradigm. We find that the anterior temporal lobe of both species possess cortical voice areas that not only prefer conspecific vocalizations but also implement a representational geometry categorizing them apart from all other sounds in a species-specific but homologous manner. These results reveal a more similar functional organization of higher-level auditory cortex in macaques and humans than currently known.

FMRI-based identity classification accuracy in left temporal and frontal regions predicts speaker recognition performance

Speaker recognition is characterized by considerable inter-individual variability with poorly understood neural bases. This study was aimed at (1) clarifying the cerebral correlates of speaker recognition in humans, in particular the involvement of prefrontal areas, using multi voxel pattern analysis (MVPA) applied to fMRI data from a relatively large group of participants, and (2) at investigating the relationship across participants between fMRI-based classification and the group’s variable behavioural performance at the speaker recognition task. A cohort of subjects (N = 40, 28 females) selected to present a wide distribution of voice recognition abilities underwent an fMRI speaker identification task during which they were asked to recognize three previously learned speakers with finger button presses. The results showed that speaker identity could be significantly decoded based on fMRI patterns in voice-sensitive regions including bilateral temporal voice areas (TVAs) along the superior temporal sulcus/gyrus but also in bilateral parietal and left inferior frontal regions. Furthermore, fMRI-based classification accuracy showed a significant correlation with individual behavioural performance in left anterior STG/STS and left inferior frontal gyrus. These results highlight the role of both temporal and extra-temporal regions in performing a speaker identity recognition task with motor responses.

Cortical voice processing is grounded in elementary sound analyses for vocalization relevant sound patterns.

A subregion of the auditory cortex (AC) was proposed to selectively process voices. This selectivity of the temporal voice area (TVA) and its role in processing non-voice sounds however have remained elusive. For a better functional description of the TVA, we investigated its neural responses both to voice and non-voice sounds, and critically also to textural sound patterns (TSPs) that share basic features with natural sounds but that are perceptually very distant from voices. Listening to these TSPs, first, elicited activity in large subregions of the TVA, which was mainly driven by perpetual ratings of TSPs along a voice similarity scale. This similar TVA activity in response to TSPs might partially explain activation patterns typically observed during voice processing. Second, we reconstructed the TVA activity that is usually observed in voice processing with a linear combination of activation patterns from TSPs. An analysis of the reconstruction model weights demonstrated that the TVA similarly processes both natural voice and non-voice sounds as well as TSPs along their acoustic and perceptual features. The predominant factor in reconstructing the TVA pattern by TSPs were the perceptual voice similarity ratings. Third, a multi-voxel pattern analysis confirms that the TSPs contain sufficient sound information to explain TVA activity for voice processing. Altogether, rather than being restricted to higher-order voice processing only, the human "voice area" uses mechanisms to evaluate the perceptual and acoustic quality of non-voice sounds, and responds to the latter with a "voice-like" processing pattern when detecting some rudimentary perceptual similarity with voices.

Adults with high functioning autism display idiosyncratic behavioral patterns, neural representations and connectivity of the ‘Voice Area’ while judging the appropriateness of emotional vocal reactions

Understanding others in everyday situations requires multiple types of information processing (visual, auditory, higher order…) which implicates the use of multiple neural circuits of the human brain. Here, using a multisensory paradigm we investigate one aspect of social understanding less explored in the literature: instead of focusing on the capacity to infer what a specific person is thinking, we explore here how people with high functioning autism (HFA) and matched controls with typical development (TD) infer the “population thinking”. For this we created an audio-visual ‘social norm inference’ task. Participants were required to imagine how most people would judge the appropriateness of vocal utterances in relation to different emotional visual contexts. Behavioral findings demonstrated that HFA individuals show more interindividual variability in these judgments despite equal within-participant reliability relative to TD. This was also the case for judgements of the valence of these vocalizations when presented in isolation. At the neural level, multivoxel pattern analysis of functional magnetic resonance imaging data revealed strikingly similar neural representations between HFA and TD participants at the group level across different hierarchical levels and neural systems. However, analyses at the individual-participant level revealed that the “Temporal Voice Area” (TVA) shows more interindividual variability in the HFA group, both for neural representations and functional connectivity. Thus, this larger neural idiosyncrasy in a high-level auditory area matches with the larger behavioral idiosyncrasy in HFA individuals, when judging auditory valence and its adequacy in different social scenarios. These results suggest that idiosyncrasy in task-relevant sensory areas in HFA participants could underlie their greater difficulties to estimate how others can think.

Large-scale plurimodal networks common to listening to, producing and reading word lists: an fMRI study combining task-induced activation and intrinsic connectivity in 144 right-handers

We aimed at identifying plurimodal large-scale networks for producing, listening to and reading word lists based on the combined analyses of task-induced activation and resting-state intrinsic connectivity in 144 healthy right-handers. In the first step, we identified the regions in each hemisphere showing joint activation and joint asymmetry during the three tasks. In the left hemisphere, 14 homotopic regions of interest (hROIs) located in the left Rolandic sulcus, precentral gyrus, cingulate gyrus, cuneus and inferior supramarginal gyrus (SMG) met this criterion, and 7 hROIs located in the right hemisphere were located in the preSMA, medial superior frontal gyrus, precuneus and superior temporal sulcus (STS). In a second step, we calculated the BOLD temporal correlations across these 21 hROIs at rest and conducted a hierarchical clustering analysis to unravel their network organization. Two networks were identified, including the WORD-LIST_CORE network that aggregated 14 motor, premotor and phonemic areas in the left hemisphere plus the right STS that corresponded to the posterior human voice area (pHVA). The present results revealed that word-list processing is based on left articulatory and storage areas supporting the action–perception cycle common not only to production and listening but also to reading. The inclusion of the right pHVA acting as a prosodic integrative area highlights the importance of prosody in the three modalities and reveals an intertwining across hemispheres between prosodic (pHVA) and phonemic (left SMG) processing. These results are consistent with the motor theory of speech postulating that articulatory gestures are the central motor units on which word perception, production, and reading develop and act together.

Spatial Cues Influence Time Estimations in Deaf Individuals.

SummaryRecent studies have reported a strong interaction between spatial and temporal representation when visual experience is missing: blind people use temporal representation of events to represent spatial metrics. Given the superiority of audition on time perception, we hypothesized that when audition is not available complex temporal representations could be impaired, and spatial representation of events could be used to build temporal metrics. To test this hypothesis, deaf and hearing subjects were tested with a visual temporal task where conflicting and not conflicting spatiotemporal information was delivered. As predicted, we observed a strong deficit of deaf participants when only temporal cues were useful and space was uninformative with respect to time. However, the deficit disappeared when coherent spatiotemporal cues were presented and increased for conflicting spatiotemporal stimuli. These results highlight that spatial cues influence time estimations in deaf participants, suggesting that deaf individuals use spatial information to infer temporal environmental coordinates.

Processing pathways for emotional vocalizations.

Emotional sounds are processed within a large cortico-subcortical network, of which the auditory cortex, the voice area, and the amygdala are the core regions. Using 7T fMRI, we have compared the effect of emotional valence (positive, neutral, and negative) and the effect of the type of environmental sounds (human vocalizations and non-vocalizations) on neural activity within individual early stage auditory areas, the voice area, and the amygdala. A two-way ANOVA was applied to the BOLD time course within each ROI. In several early stage auditory areas, it yielded a significant main effect of vocalizations and of valence, but not a significant interaction. Significant interaction as well as significant main effects of vocalization and of valence were present in the voice area; the former was driven by a significant emotional modulation of vocalizations but not of other sounds. Within the amygdala, only the main effect of valence was significant. Post-hoc correlation analysis highlighted coupling between the voice area and early stage auditory areas during the presentation of any vocalizations, and between the voice area and the right amygdala during positive vocalizations. Thus, the voice area is selectively devoted to the encoding of the emotional valence of vocalizations; it shares with several early stage auditory areas encoding characteristics for vocalizations and with the amygdala for the emotional modulation of vocalizations. These results are indicative of a dual pathway, whereby the emotional modulation of vocalizations within the voice area integrates the input from the lateral early stage auditory areas and from the amygdala.

What and How the Deaf Brain Sees.

Over the past decade, there has been an unprecedented level of interest and progress into understanding visual processing in the brain of the deaf. Specifically, when the brain is deprived of input from one sensory modality (such as hearing), it often compensates with supranormal performance in one or more of the intact sensory systems (such as vision). Recent psychophysical, functional imaging, and reversible deactivation studies have converged to define the specific visual abilities that are enhanced in the deaf, as well as the cortical loci that undergo crossmodal plasticity in the deaf and are responsible for mediating these superior visual functions. Examination of these investigations reveals that central visual functions, such as object and facial discrimination, and peripheral visual functions, such as motion detection, visual localization, visuomotor synchronization, and Vernier acuity (measured in the periphery), are specifically enhanced in the deaf, compared with hearing participants. Furthermore, the cortical loci identified to mediate these functions reside in deaf auditory cortex: BA 41, BA 42, and BA 22, in addition to the rostral area, planum temporale, Te3, and temporal voice area in humans; primary auditory cortex, anterior auditory field, dorsal zone of auditory cortex, auditory field of the anterior ectosylvian sulcus, and posterior auditory field in cats; and primary auditory cortex and anterior auditory field in both ferrets and mice. Overall, the findings from these studies show that crossmodal reorganization in auditory cortex of the deaf is responsible for the superior visual abilities of the deaf.

Tuned to voices and faces: Cerebral responses linked to social anxiety

Voices and faces are the most common sources of threat in social anxiety (SA) where the fear of negative evaluation and social exclusion is the central element. SA itself is spectrally distributed among the general population and its clinical manifestation, termed social anxiety disorder, is one of the most common anxiety disorders. While heightened cerebral responses to angry or contemptuous facial or vocal expressions are well documented, it remains unclear if the brain of socially anxious individuals is generally more sensitive to voices and faces. Using functional magnetic resonance imaging, we investigated how SA affects the cerebral processing of voices and faces as compared to various other stimulus types in a study population with greatly varying SA (N = 50, 26 female). While cerebral voice-sensitivity correlated positively with SA in the left temporal voice area (TVA) and the left amygdala, an association of face-sensitivity and SA was observed in the right fusiform face area (FFA) and the face processing area of the right posterior superior temporal sulcus (pSTSFA). These results demonstrate that the increase of cerebral responses associated with social anxiety is not limited to facial or vocal expressions of social threat but that the respective sensory and emotion processing structures are also generally tuned to voices and faces.

CACNA1C risk variant affects microstructural connectivity of the amygdala.

Deficits in perception of emotional prosody have been described in patients with affective disorders at behavioral and neural level. In the current study, we use an imaging genetics approach to examine the impact of CACNA1C, one of the most promising genetic risk factors for psychiatric disorders, on prosody processing on a behavioral, functional and microstructural level. Using functional magnetic resonance imaging (fMRI) and diffusion tensor imaging (DTI) we examined key areas involved in prosody processing, i.e. the amygdala and voice areas, in a healthy population. We found stronger activation to emotional than neutral prosody in the voice areas and the amygdala, but CACNA1C rs1006737 genotype had no influence on fMRI activity. However, significant microstructural differences (i.e. mean diffusivity) between CACNA1C rs1006737 risk allele carriers and non carriers were found in the amygdala, but not the voice areas. These modifications in brain architecture associated with CACNA1C might reflect a neurobiological marker predisposing to affective disorders and concomitant alterations in emotion perception.

Speech-Language Pathologists with a PHD in Brazil: profile of professional training and scientific production in the voice area

ABSTRACT Purpose: To investigate, among the Brazilian Speech-Language Pathologists with a doctoral degree, who analyzed voice-related aspects in their theses, the variables gender, year of defense of the thesis, type and location of the educational institution, inclusion of the program through which the thesis was developed, thesis’ theme and the authors' scientific production in the last 10 years. Methods: data collected through a survey on the Lattes Platform from 1986 to 2017. Inclusion criteria were having a degree in Speech-Language Pathology, being Brazilian and having a doctoral degree. The variables defined were recorded in the STATA/IC 14.2, a descriptive analysis of the data was performed, and the growth trend of the number of theses was determined. Results: Most of the 104 professionals who composed the sample were females, with a doctoral degree from a federal public institution located in the Southeast region, and who defended a thesis related to Clinical Voice in specific programs in the area (Human Communication Disorders; Speech-Language Pathology; Speech-Language Pathology, Physical therapy and Occupational Therapy). Article production included 1,458 articles published in the analyzed period, with 6,867 citations in various databases. Conclusion: There has been a steady growth in the number of theses defended in the voice area in the last 30 years, but still concentrated on clinical voice sub-areas, in federal public institutions, predominantly in the Brazilian Southeast region, and in specific programs for Speech-Language Pathology.

Cerebral resting state markers of biased perception in social anxiety.

Social anxiety (SA) comprises a multitude of persistent fears around the central element of dreaded negative evaluation and exclusion. This very common anxiety is spectrally distributed among the general population and associated with social perception biases deemed causal in its maintenance. Here, we investigated cerebral resting state markers linking SA and biased social perception. To this end, resting state functional connectivity (RSFC) was assessed as the neurobiological marker in a study population with greatly varying SA using fMRI in the first step of the experiment. One month later the impact of unattended laughter-exemplifying social threat-on a face rating task was evaluated as a measure of biased social perception. Applying a dimensional approach, SA-related cognitive biases tied to the valence, dominance and arousal of the threat signal and their underlying RSFC patterns among central nodes of the cerebral emotion, voice and face processing networks were identified. In particular, the connectivity patterns between the amygdalae and the right temporal voice area met all criteria for a cerebral mediation of the association between SA and the laughter valence-related interpretation bias. Thus, beyond this identification of non-state-dependent cerebral markers of biased perception in SA, this study highlights both a starting point and targets for future research on the causal relationships between cerebral connectivity patterns, SA and biased perception, potentially via neurofeedback methods.

Hierarchical Brain Network for Face and Voice Integration of Emotion Expression

The brain has separate specialized computational units to process faces and voices located in occipital and temporal cortices. However, humans seamlessly integrate signals from the faces and voices of others for optimal social interaction. How are emotional expressions, when delivered by different sensory modalities (faces and voices), integrated in the brain? In this study, we characterized the brains' response to faces, voices, and combined face-voice information (congruent, incongruent), which varied in expression (neutral, fearful). Using a whole-brain approach, we found that only the right posterior superior temporal sulcus (rpSTS) responded more to bimodal stimuli than to face or voice alone but only when the stimuli contained emotional expression. Face- and voice-selective regions of interest, extracted from independent functional localizers, similarly revealed multisensory integration in the face-selective rpSTS only; further, this was the only face-selective region that also responded significantly to voices. Dynamic causal modeling revealed that the rpSTS receives unidirectional information from the face-selective fusiform face area, and voice-selective temporal voice area, with emotional expression affecting the connection strength. Our study promotes a hierarchical model of face and voice integration, with convergence in the rpSTS, and that such integration depends on the (emotional) salience of the stimuli.

Aggression modulates neural correlates of hostile intention attribution to laughter in children

The tendency to interpret nonverbal social signals as hostile in intention is associated with aggressive responding, poor social functioning and mental illness, and can already be observed in childhood. To investigate the neural correlates of such hostile attributions of social intention, we performed a functional magnetic imaging study in 10–18 year old children and adolescents. Fifty healthy participants rated videos of laughter, which they were told to imagine as being directed towards them, as friendly versus hostile in social intention. Hostile intention ratings were associated with neural response in the right temporal voice area (TVA). Moreover, self-reported trait physical aggression modulated this relationship in both the right TVA and bilateral lingual gyrus, with stronger associations between hostile intention ratings and neural activation in children with higher trait physical aggression scores. Functional connectivity results showed decreased connectivity between the right TVA and left dorsolateral prefrontal cortex with increasing trait physical aggression for making hostile social intention attributions. We conclude that children's social intention attributions are more strongly related to activation of early face and voice-processing regions with increasing trait physical aggression.

Functional connectivity within the voice perception network and its behavioural relevance

Recognizing 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 = 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.

White matter connectivity between occipital and temporal regions involved in face and voice processing in hearing and early deaf individuals

Neuroplasticity following sensory deprivation has long inspired neuroscience research in the quest of understanding how sensory experience and genetics interact in developing the brain functional and structural architecture. Many studies have shown that sensory deprivation can lead to cross-modal functional recruitment of sensory deprived cortices. Little is known however about how structural reorganization may support these functional changes. In this study, we examined early deaf, hearing signer and hearing non-signer individuals using diffusion MRI to evaluate the potential structural connectivity linked to the functional recruitment of the temporal voice area by face stimuli in deaf individuals. More specifically, we characterized the structural connectivity between occipital, fusiform and temporal regions typically supporting voice- and face-selective processing. Despite the extensive functional reorganization for face processing in the temporal cortex of the deaf, macroscopic properties of these connections did not differ across groups. However, both occipito- and fusiform-temporal connections showed significant microstructural changes between groups (fractional anisotropy reduction, radial diffusivity increase). We propose that the reorganization of temporal regions after early auditory deprivation builds on intrinsic and mainly preserved anatomical connectivity between functionally specific temporal and occipital regions.

Assessment of voice, speech and communication changes associated with cervical spinal cord injury.

Respiratory muscle impairment following cervical spinal cord injury (CSCI) may lead to reduced voice function, although the individual variation is large. Voice problems in this population may not always receive attention since individuals with CSCI face other, more acute and life-threatening issues that need/receive attention. Currently there is no consensus on the tasks suitable to identify the specific voice impairments and functional voice changes experienced by individuals with CSCI. To examine which voice/speech tasks identify the specific voice and communication changes associated with CSCI, habitual and maximum speech performance of a group with CSCI was compared with that of a healthy control group (CG), and the findings were related to respiratory function and to self-reported voice problems. Respiratory, aerodynamic, acoustic and self-reported voice data from 19 individuals (nine women and 10 men, aged 23-59 years, heights = 153-192 cm) with CSCI (levels C3-C7) were compared with data from a CG consisting of 19 carefully matched non-injured people (nine women and 10 men, aged 19-59 years, heights = 152-187 cm). Despite considerable variability of performance, highly significant differences between the group with CSCI and the CG were found in maximum phonation time, maximum duration of breath phrases, maximum sound pressure level and maximum voice area in voice-range profiles (all p = .000). Subglottal pressure was lower and phonatory stability was reduced in some of the individuals with CSCI, but differences between the groups were not statistically significant. Six of 19 had voice handicap index (VHI) scores above 20 (the cut-off for voice disorder). Individuals with a vital capacity below 50% of the expected for an equivalent reference individual performed significantly worse than participants with more normal vital capacity. Completeness and level of injury seemed to impact vocal function in some individuals. A combination of maximum performance speech tasks, respiratory tasks and self-reported information on voice problems help to identify individuals with reduced voice function following CSCI. Early identification of individuals with voice changes post-CSCI, and introducing appropriate rehabilitation strategies, may help to minimize development of maladaptive voice behaviours such as vocal strain, which can lead to further impairments and limitations to communication participation.

Neurobiological correlates of emotional intelligence in voice and face perception networks.

Facial expressions and voice modulations are among the most important communicational signals to convey emotional information. The ability to correctly interpret this information is highly relevant for successful social interaction and represents an integral component of emotional competencies that have been conceptualized under the term emotional intelligence. Here, we investigated the relationship of emotional intelligence as measured with the Salovey-Caruso-Emotional-Intelligence-Test (MSCEIT) with cerebral voice and face processing using functional and structural magnetic resonance imaging. MSCEIT scores were positively correlated with increased voice-sensitivity and gray matter volume of the insula accompanied by voice-sensitivity enhanced connectivity between the insula and the temporal voice area, indicating generally increased salience of voices. Conversely, in the face processing system, higher MSCEIT scores were associated with decreased face-sensitivity and gray matter volume of the fusiform face area. Taken together, these findings point to an alteration in the balance of cerebral voice and face processing systems in the form of an attenuated face-vs-voice bias as one potential factor underpinning emotional intelligence.

Perceptual-Auditory and Acoustical Analysis of the Voices of Transgender Women

Voice is an important gender marker in the transition process as a transgender individual accepts a new gender identity. The objectives of this study were to describe and relate aspects of a perceptual-auditory analysis and the fundamental frequency (F0) of male-to-female (MtF) transsexual individuals. A case-control study was carried out with individuals aged 19-52 years who attended the Gender Identity Program of the Hospital de Clínicas of Porto Alegre. Vocal recordings from the MtF transgender and cisgender individuals (vowel /a:/ and six phrases of Consensus Auditory Perceptual Evaluation Voice [CAPE-V]) were edited and randomly coded before storage in a Dropbox folder. The voices (vowel /a:/) were analyzed by consensus on the same day by two judge speech therapists who had more than 10 years of experience in the voice area using the GRBASI perceptual-auditory vocal evaluation scale. Acoustic analysis of the voices was performed using the advanced Multi-Dimensional Voice Program software. The resonance focus and the degrees of masculinity and femininity for each voice recording were determined by listening to the CAPE-V phrases, for the same judges. There were significant differences between the groups regarding a greater frequency of subjects with F0 between 80 and 150 Hz (P = 0.003), and a greater frequency of hypernasal resonant focus (P < 0.001) in the MtF cases and greater frequency of subjects with absence of roughness (P = 0.031) in the control group. The MtF group of individuals showed altered vertical resonant focus, more masculine voices, and lower fundamental frequencies. The control group showed a significant absence of roughness.

Voice selectivity in the temporal voice area despite matched low-level acoustic cues

In human listeners, the temporal voice areas (TVAs) are regions of the superior temporal gyrus and sulcus that respond more to vocal sounds than a range of nonvocal control sounds, including scrambled voices, environmental noises, and animal cries. One interpretation of the TVA’s selectivity is based on low-level acoustic cues: compared to control sounds, vocal sounds may have stronger harmonic content or greater spectrotemporal complexity. Here, we show that the right TVA remains selective to the human voice even when accounting for a variety of acoustical cues. Using fMRI, single vowel stimuli were contrasted with single notes of musical instruments with balanced harmonic-to-noise ratios and pitches. We also used “auditory chimeras”, which preserved subsets of acoustical features of the vocal sounds. The right TVA was preferentially activated only for the natural human voice. In particular, the TVA did not respond more to artificial chimeras preserving the exact spectral profile of voices. Additional acoustic measures, including temporal modulations and spectral complexity, could not account for the increased activation. These observations rule out simple acoustical cues as a basis for voice selectivity in the TVAs.