Voice Area Research Articles

Early neurophysiological correlates of vocal versus non-vocal sound processing in adults

Electrophysiological correlates of voice processing were studied in twenty adults by comparing auditory evoked potentials in response to voice and environmental sounds in passive condition. Both categories of stimuli elicited similar cortical auditory responses (i.e. N1, P2, N2 peaks); however these peaks were overlapped by two components specifically elicited by voice. The first component was evidenced as a positive deflection recorded over the fronto-temporal sites, and lateralized on the right hemiscalp. This fronto-temporal positivity to voice (FTPV) may constitute the electrophysiological counterpart of the activation of the temporal voice areas previously described in neuroimaging studies. The second component was recorded at occipito-temporo-parietal sites. This occipito–temporo–parietal negativity to voice might correspond to visual mental imagery of the vocal sounds or to some form of mental simulation of the action sounds (e.g. coughing). Both components began as early as 70ms post-stimulus onset indicating a rapid discrimination of voice in our auditory environment, which might be the basis of communication functions in humans.

Norm-Based Coding of Voice Identity in Human Auditory Cortex

SummaryListeners exploit small interindividual variations around a generic acoustical structure to discriminate and identify individuals from their voice—a key requirement for social interactions. The human brain contains temporal voice areas (TVA) [1] involved in an acoustic-based representation of voice identity [2, 3, 4, 5, 6], but the underlying coding mechanisms remain unknown. Indirect evidence suggests that identity representation in these areas could rely on a norm-based coding mechanism [4, 7, 8, 9, 10, 11]. Here, we show by using fMRI that voice identity is coded in the TVA as a function of acoustical distance to two internal voice prototypes (one male, one female)—approximated here by averaging a large number of same-gender voices by using morphing [12]. Voices more distant from their prototype are perceived as more distinctive and elicit greater neuronal activity in voice-sensitive cortex than closer voices—a phenomenon not merely explained by neuronal adaptation [13, 14]. Moreover, explicit manipulations of distance-to-mean by morphing voices toward (or away from) their prototype elicit reduced (or enhanced) neuronal activity. These results indicate that voice-sensitive cortex integrates relevant acoustical features into a complex representation referenced to idealized male and female voice prototypes. More generally, they shed light on remarkable similarities in cerebral representations of facial and vocal identity.

Functional responses and structural connections of cortical areas for processing faces and voices in the superior temporal sulcus

It was the aim of this study to delineate the areas along the right superior temporal sulcus (STS) for processing of faces, voices, and face-voice integration using established functional magnetic resonance imaging (fMRI) localizers and to assess their structural connectivity profile with diffusion tensor imaging (DTI). We combined this approach with an fMRI adaptation design during which the participants judged emotions in facial expressions and prosody and demonstrated response habituation in the orbitofrontal cortex (OFC) which occurred irrespective of the sensory modality. These functional data were in line with DTI findings showing separable fiber projections of the three different STS modules converging in the OFC which run through the external capsule for the voice area, through the dorsal superior longitudinal fasciculus (SLF) for the face area and through the ventral SLF for the audiovisual integration area. The OFC was structurally connected with the supplementary motor area (SMA) and activation in these two areas was correlated with faster stimulus evaluation during repetition priming. Based on these structural and functional properties, we propose that the OFC is part of the extended system for perception of emotional information in faces and voices and constitutes a neural interface linking sensory areas with brain regions implicated in generation of behavioral responses.

How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading

As you might experience it while reading this sentence, silent reading often involves an imagery speech component: we can hear our own "inner voice" pronouncing words mentally. Recent functional magnetic resonance imaging studies have associated that component with increased metabolic activity in the auditory cortex, including voice-selective areas. It remains to be determined, however, whether this activation arises automatically from early bottom-up visual inputs or whether it depends on late top-down control processes modulated by task demands. To answer this question, we collaborated with four epileptic human patients recorded with intracranial electrodes in the auditory cortex for therapeutic purposes, and measured high-frequency (50-150 Hz) "gamma" activity as a proxy of population level spiking activity. Temporal voice-selective areas (TVAs) were identified with an auditory localizer task and monitored as participants viewed words flashed on screen. We compared neural responses depending on whether words were attended or ignored and found a significant increase of neural activity in response to words, strongly enhanced by attention. In one of the patients, we could record that response at 800 ms in TVAs, but also at 700 ms in the primary auditory cortex and at 300 ms in the ventral occipital temporal cortex. Furthermore, single-trial analysis revealed a considerable jitter between activation peaks in visual and auditory cortices. Altogether, our results demonstrate that the multimodal mental experience of reading is in fact a heterogeneous complex of asynchronous neural responses, and that auditory and visual modalities often process distinct temporal frames of our environment at the same time.

Incomplete Swallowing and Retracted Tongue Maneuvers for Electromyographic Signal Normalization of the Extrinsic Muscles of the Larynx

To investigate which muscular maneuvers provide larger electric activity (EA) of the suprahyoid (SH) and infrahyoid (IH) muscles to be used as surface electromyography (SEMG) signal normalization reference. The electrical potentials of the SH and IH muscles of 12 subjects were evaluated using six muscular maneuvers, involving the position of the tongue and effort. It was selected as maximum voluntary sustained activity maneuver, the one having the minor coefficient of variation and the smallest value for each muscle group. The EA signal was converted using the root mean square in microvolts. It was considered then the maximum signal of each maneuver as the difference between the mean of three measures and the resting potential. The maneuvers that provided higher mean potentials with minor coefficient of variation and smallest P value were incomplete swallowing (IS) with effort (mean potential equal to 56.73±8.68 with coefficient of variation of 15.30%) in SH group, and tongue retracted with mouth open (TROM, mean potential equal to 46.57±7.83 with coefficient of variation of 16.81%) in IH group. The IS with effort and TROM maneuvers should be considered for signal normalization in these muscles, respectively, and may provide conditions for using the SEMG in voice clinic. The use of normalization standards in researches of SH and IH muscles in the voice area will allow comparisons among future works.

The Early Spatio-Temporal Correlates and Task Independence of Cerebral Voice Processing Studied with MEG

Functional magnetic resonance imaging studies have repeatedly provided evidence for temporal voice areas (TVAs) with particular sensitivity to human voices along bilateral mid/anterior superior temporal sulci and superior temporal gyri (STS/STG). In contrast, electrophysiological studies of the spatio-temporal correlates of cerebral voice processing have yielded contradictory results, finding the earliest correlates either at ∼300-400 ms, or earlier at ∼200 ms ("fronto-temporal positivity to voice", FTPV). These contradictory results are likely the consequence of different stimulus sets and attentional demands. Here, we recorded magnetoencephalography activity while participants listened to diverse types of vocal and non-vocal sounds and performed different tasks varying in attentional demands. Our results confirm the existence of an early voice-preferential magnetic response (FTPVm, the magnetic counterpart of the FTPV) peaking at about 220 ms and distinguishing between vocal and non-vocal sounds as early as 150 ms after stimulus onset. The sources underlying the FTPVm were localized along bilateral mid-STS/STG, largely overlapping with the TVAs. The FTPVm was consistently observed across different stimulus subcategories, including speech and non-speech vocal sounds, and across different tasks. These results demonstrate the early, largely automatic recruitment of focal, voice-selective cerebral mechanisms with a time-course comparable to that of face processing.

Cerebral integration of verbal and nonverbal emotional cues: Impact of individual nonverbal dominance

Emotional communication is essential for successful social interactions. Emotional information can be expressed at verbal and nonverbal levels. If the verbal message contradicts the nonverbal expression, usually the nonverbal information is perceived as being more authentic, revealing the "true feelings" of the speaker. The present fMRI study investigated the cerebral integration of verbal (sentences expressing the emotional state of the speaker) and nonverbal (facial expressions and tone of voice) emotional signals using ecologically valid audiovisual stimulus material. More specifically, cerebral activation associated with the relative impact of nonverbal information on judging the affective state of a speaker (individual nonverbal dominance index, INDI) was investigated. Perception of nonverbally expressed emotions was associated with bilateral activation within the amygdala, fusiform face area (FFA), temporal voice area (TVA), and the posterior temporal cortex as well as in the midbrain and left inferior orbitofrontal cortex (OFC)/left insula. Verbally conveyed emotions were linked to increased responses bilaterally in the TVA. Furthermore, the INDI correlated with responses in the left amygdala elicited by nonverbal and verbal emotional stimuli. Correlation of the INDI with the activation within the medial OFC was observed during the processing of communicative signals. These results suggest that individuals with a higher degree of nonverbal dominance have an increased sensitivity not only to nonverbal but to emotional stimuli in general.

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

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.

Brain ‘talks over’ boring quotes: Top-down activation of voice-selective areas while listening to monotonous direct speech quotations

In human communication, direct speech (e.g., Mary said, "I'm hungry") is perceived as more vivid than indirect speech (e.g., Mary said that she was hungry). This vividness distinction has previously been found to underlie silent reading of quotations: Using functional magnetic resonance imaging (fMRI), we found that direct speech elicited higher brain activity in the temporal voice areas (TVA) of the auditory cortex than indirect speech, consistent with an "inner voice" experience in reading direct speech. Here we show that listening to monotonously spoken direct versus indirect speech quotations also engenders differential TVA activity. This suggests that individuals engage in top-down simulations or imagery of enriched supra-segmental acoustic representations while listening to monotonous direct speech. The findings shed new light on the acoustic nature of the "inner voice" in understanding direct speech.

Sound-induced activity in voice-sensitive cortex predicts voice memory ability.

The “temporal voice areas” (TVAs; Belin et al., 2000) of the human brain show greater neuronal activity in response to human voices than to other categories of non-vocal sounds. However, a direct link between TVA activity and voice perception behavior has not yet been established. Here we show that a functional magnetic resonance imaging measure of activity in the TVAs predicts individual performance at a separately administered voice memory test. This relation holds when general sound memory ability is taken into account. These findings provide the first evidence that the TVAs are specifically involved in voice cognition.

Effects of vocoding and intelligibility on the cerebral response to speech

BackgroundDegrading speech through an electronic synthesis technique called vocoding has been shown to affect cerebral processing of speech in several cortical areas. However, it is not clear whether the effects of speech degradation by vocoding are related to acoustical degradation or by the associated loss in intelligibility. Using vocoding and a parametric variation of the number of frequency bands used for the encoding, we investigated the effects of the degradation of auditory spectral content on cerebral processing of intelligible speech (words), unintelligible speech (words in a foreign language), and complex environmental sounds.ResultsVocoding was found to decrease activity to a comparable degree for intelligible and unintelligible speech in most of the temporal lobe. Only the bilateral posterior temporal areas showed a significant interaction between vocoding and intelligibility, with a stronger vocoding-induced decrease in activity for intelligible speech. Comparisons to responses elicited by environmental sounds showed that portions of the temporal voice areas (TVA) retained their greater responses to voice even under adverse listening conditions. The recruitment of specific networks in temporal regions during exposure to degraded speech follows a radial and anterior-posterior topography compared to the networks recruited by exposure to speech that is not degraded.ConclusionsDifferent brain networks are involved in vocoded sound processing of intelligible speech, unintelligible speech, and non-vocal sounds. The greatest differences are between speech and environmental sounds, which could be related to the distinctive temporal structure of speech sounds.

Right temporal TMS impairs voice detection

Summary Functional magnetic resonance imaging (fMRI) research has revealed bilateral cortical regions along the upper banks of the superior temporal sulci (STS) which respond preferentially to voices compared to non-vocal, environmental sounds [1,2]. This sensitivity is particularly pronounced in the right hemisphere. Voice perception models imply that these regions, referred to as the temporal voice areas (TVAs), could correspond to a first stage of voice-specific processing in auditory cortex [3,4], after which different types of vocal information are processed in interacting but partially independent functional pathways. However, clear causal evidence for this claim is missing. Here we provide the first direct link between TVA activity and voice detection ability using repetitive transcranial magnetic stimulation (rTMS). Voice/non-voice discrimination ability was impaired when rTMS was targeted at the right TVA compared with a control site. In contrast, a lower-level loudness judgement task was not differentially affected by site of stimulation. Results imply that neuronal computations in the right TVA are necessary for the distinction between human voices and other, non-vocal sounds.

Emotional Voice Areas: Anatomic Location, Functional Properties, and Structural Connections Revealed by Combined fMRI/DTI

We determined the location, functional response profile, and structural fiber connections of auditory areas with voice- and emotion-sensitive activity using functional magnetic resonance imaging (fMRI) and diffusion tensor imaging. Bilateral regions responding to emotional voices were consistently found in the superior temporal gyrus, posterolateral to the primary auditory cortex. Event-related fMRI showed stronger responses in these areas to voices-expressing anger, sadness, joy, and relief, relative to voices with neutral prosody. Their neural responses were primarily driven by prosodic arousal, irrespective of valence. Probabilistic fiber tracking revealed direct structural connections of these "emotional voice areas" (EVA) with ipsilateral medial geniculate body, which is the major input source of early auditory cortex, as well as with the ipsilateral inferior frontal gyrus (IFG) and inferior parietal lobe (IPL). In addition, vocal emotions (compared with neutral prosody) increased the functional coupling of EVA with the ipsilateral IFG but not IPL. These results provide new insights into the neural architecture of the human voice processing system and support a crucial involvement of IFG in the recognition of vocal emotions, whereas IPL may subserve distinct auditory spatial functions, consistent with distinct anatomical substrates for the processing of "how" and "where" information within the auditory pathways.

Evolution of crossmodal reorganization of the voice area in cochlear‐implanted deaf patients

Psychophysical and neuroimaging studies in both animal and human subjects have clearly demonstrated that cortical plasticity following sensory deprivation leads to a brain functional reorganization that favors the spared modalities. In postlingually deaf patients, the use of a cochlear implant (CI) allows a recovery of the auditory function, which will probably counteract the cortical crossmodal reorganization induced by hearing loss. To study the dynamics of such reversed crossmodal plasticity, we designed a longitudinal neuroimaging study involving the follow-up of 10 postlingually deaf adult CI users engaged in a visual speechreading task. While speechreading activates Broca's area in normally hearing subjects (NHS), the activity level elicited in this region in CI patients is abnormally low and increases progressively with post-implantation time. Furthermore, speechreading in CI patients induces abnormal crossmodal activations in right anterior regions of the superior temporal cortex normally devoted to processing human voice stimuli (temporal voice-sensitive areas-TVA). These abnormal activity levels diminish with post-implantation time and tend towards the levels observed in NHS. First, our study revealed that the neuroplasticity after cochlear implantation involves not only auditory but also visual and audiovisual speech processing networks. Second, our results suggest that during deafness, the functional links between cortical regions specialized in face and voice processing are reallocated to support speech-related visual processing through cross-modal reorganization. Such reorganization allows a more efficient audiovisual integration of speech after cochlear implantation. These compensatory sensory strategies are later completed by the progressive restoration of the visuo-audio-motor speech processing loop, including Broca's area.

Learning-Induced Changes in the Cerebral Processing of Voice Identity

Temporal voice areas showing a larger activity for vocal than non-vocal sounds have been identified along the superior temporal sulcus (STS); more voice-sensitive areas have been described in frontal and parietal lobes. Yet, the role of voice-sensitive regions in representing voice identity remains unclear. Using a functional magnetic resonance adaptation design, we aimed at disentangling acoustic- from identity-based representations of voices. Sixteen participants were scanned while listening to pairs of voices drawn from morphed continua between 2 initially unfamiliar voices, before and after a voice learning phase. In a given pair, the first and second stimuli could be identical or acoustically different and, at the second session, perceptually similar or different. At both sessions, right mid-STS/superior temporal gyrus (STG) and superior temporal pole (sTP) showed sensitivity to acoustical changes. Critically, voice learning induced changes in the acoustical processing of voices in inferior frontal cortices (IFCs). At the second session only, right IFC and left cingulate gyrus showed sensitivity to changes in perceived identity. The processing of voice identity appears to be subserved by a large network of brain areas ranging from the sTP, involved in an acoustic-based representation of unfamiliar voices, to areas along the convexity of the IFC for identity-related processing of familiar voices.

Voice discrimination in cochlear-implanted deaf subjects

The human voice is important for social communication because voices carry speech and other information such as a person’s physical characteristics and affective state. Further restricted temporal cortical regions are specifically involved in voice processing. In cochlear-implanted deaf patients, the processor alters the spectral cues which are crucial for the perception of the paralinguistic information of human voices. The aim of this study was to assess the abilities of voice discrimination in cochlear-implant (CI) users and in normal-hearing subjects (NHS) using a CI simulation (vocoder). In NHS the performance in voice discrimination decreased when reducing the spectral information by decreasing the number of channels of the vocoder. In CI patients with different delays after implantation we observed a strong impairment in voice discrimination at time of activation of the neuroprosthesis. No significant improvement can be detected in patients after two years of experience of the implant while they have reached a higher level of recovery of speech perception, suggesting a dissociation in the dynamic of functional recuperation of speech and voice processing. In addition to the lack of spectral cues due to the implant processor, we hypothesized that the origin of such deficit could derive from a crossmodal reorganization of the temporal voice areas in CI patients.

Spectral quality of light modulates emotional brain responses in humans

Light therapy can be an effective treatment for mood disorders, suggesting that light is able to affect mood state in the long term. As a first step to understand this effect, we hypothesized that light might also acutely influence emotion and tested whether short exposures to light modulate emotional brain responses. During functional magnetic resonance imaging, 17 healthy volunteers listened to emotional and neutral vocal stimuli while being exposed to alternating 40-s periods of blue or green ambient light. Blue (relative to green) light increased responses to emotional stimuli in the voice area of the temporal cortex and in the hippocampus. During emotional processing, the functional connectivity between the voice area, the amygdala, and the hypothalamus was selectively enhanced in the context of blue illumination, which shows that responses to emotional stimulation in the hypothalamus and amygdala are influenced by both the decoding of vocal information in the voice area and the spectral quality of ambient light. These results demonstrate the acute influence of light and its spectral quality on emotional brain processing and identify a unique network merging affective and ambient light information.

The Brain’s Voices: Comparing Nonclinical Auditory Hallucinations and Imagery

Although auditory verbal hallucinations are often thought to denote mental illness, the majority of voice hearers do not satisfy the criteria for a psychiatric disorder. Here, we report the first functional imaging study of such nonclinical hallucinations in 7 healthy voice hearers comparing them with auditory imagery. The human voice area in the superior temporal sulcus was activated during both hallucinations and imagery. Other brain areas supporting both hallucinations and imagery included fronto temporal language areas in the left hemisphere and their contralateral homologues and the supplementary motor area (SMA). Hallucinations are critically distinguished from imagery by lack of voluntary control. We expected this difference to be reflected in the relative timing of prefrontal and sensory areas. Activity of the SMA indeed preceded that of auditory areas during imagery, whereas during hallucinations, the 2 processes occurred instantaneously. Voluntary control was thus represented in the relative timing of prefrontal and sensory activation, whereas the sense of reality of the sensory experience may be a product of the voice area activation. Our results reveal mechanisms of the generation of sensory experience in the absence of external stimulation and suggest new approaches to the investigation of the neurobiology of psychopathology.

The Singer's Voice Range Profile: Female Professional Opera Soloists

This work concerns the collection of 30 voice range profiles (VRPs) of female operatic voice. We address the questions: Is there a need for a singer's protocol in VRP acquisition? Are physiological measurements sufficient or should the measurement of performance capabilities also be included? Can we address the female singing voice in general or is there a case for categorizing voices when studying phonetographic data? Subjects performed a series of structured tasks involving both standard speech voice protocols and additional singing tasks. Singers also completed an extensive questionnaire. Physiological VRPs differ from performance VRPs. Two new VRP metrics, the voice area above a defined level threshold and the dynamic range independent from the fundamental frequency (F(0)), were found to be useful in the analysis of singer VRPs. Task design had no effect on performance VRP outcomes. Voice category differences were mainly attributable to phonation frequency-based information. Results support the clinical importance of addressing the vocal instrument as it is used in performance. Equally important is the elaboration of a protocol suitable for the singing voice. The given context and instructions can be more important than task design for performance VRPs. Yet, for physiological VRP recordings, task design remains critical. Both types of VRPs are suggested for a singer's voice evaluation.

Auditory response of the Temporal Voice Areas (TVA) predicts memory performance for voices, but not bells.

Auditory response of the Temporal Voice Areas (TVA) predicts memory performance for voices, but not bells.