Visual mechanisms for voice‐identity recognition flexibly adjust to auditory noise level

Recognising the identity of voices is a key ingredient of communication. Visual mechanisms support this ability: recognition is better for voices previously learned with their corresponding face (compared to a control condition). This so-called 'face-benefit' is supported by the fusiform face area (FFA), a region sensitive to facial form and identity. Behavioural findings indicate that the face-benefit increases in noisy listening conditions. The neural mechanisms for this increase are unknown. Here, using functional magnetic resonance imaging, we examined responses in face-sensitive regions while participants recognised the identity of auditory-only speakers (previously learned by face) in high (SNR -4 dB) and low (SNR +4 dB) levels of auditory noise. We observed a face-benefit in both noise levels, for most participants (16 of 21). In high-noise, the recognition of face-learned speakers engaged the right posterior superior temporal sulcus motion-sensitive face area (pSTS-mFA), a region implicated in the processing of dynamic facial cues. The face-benefit in high-noise also correlated positively with increased functional connectivity between this region and voice-sensitive regions in the temporal lobe in the group of 16 participants with a behavioural face-benefit. In low-noise, the face-benefit was robustly associated with increased responses in the FFA and to a lesser extent the right pSTS-mFA. The findings highlight the remarkably adaptive nature of the visual network supporting voice-identity recognition in auditory-only listening conditions

Responses in left inferior frontal gyrus are altered for speech‐in‐noise processing, but not for clear speech in autism

Introduction: Autistic individuals often have difficulties with recognizing what another person is saying in noisy conditions such as in a crowded classroom or a restaurant. The underlying neural mechanisms of this speech perception difficulty are unclear. In typically developed individuals, three cerebral cortex regions are particularly related to speech-in-noise perception: the left inferior frontal gyrus (IFG), the right insula, and the left inferior parietal lobule (IPL). Here, we tested whether responses in these cerebral cortex regions are altered in speech-in-noise perception in autism.Methods: Seventeen autistic adults and 17 typically developed controls (matched pairwise on age, sex, and IQ) performed an auditory-only speech recognition task during functional magnetic resonance imaging (fMRI). Speech was presented either with noise (noise condition) or without noise (no noise condition, i.e., clear speech).Results: In the left IFG, blood-oxygenation-level-dependent (BOLD) responses were higher in the control compared to the autism group for recognizing speech-in-noise compared to clear speech. For this contrast, both groups had similar response magnitudes in the right insula and left IPL. Additionally, we replicated previous findings that BOLD responses in speech-related and auditory brain regions (including bilateral superior temporal sulcus and Heschl's gyrus) for clear speech were similar in both groups and that voice identity recognition was impaired for clear and noisy speech in autism.Discussion: Our findings show that in autism, the processing of speech is particularly reduced under noisy conditions in the left IFG-a dysfunction that might be important in explaining restricted speech comprehension in noisy environments

Adjudicating between local and global architectures of predictive processing in the subcortical auditory pathway

Predictive processing, a leading theoretical framework for sensory processing, suggests that the brain constantly generates predictions on the sensory world and that perception emerges from the comparison between these predictions and the actual sensory input. This requires two distinct neural elements: generative units, which encode the model of the sensory world; and prediction error units, which compare these predictions against the sensory input. Although predictive processing is generally portrayed as a theory of cerebral cortex function, animal and human studies over the last decade have robustly shown the ubiquitous presence of prediction error responses in several nuclei of the auditory, somatosensory, and visual subcortical pathways. In the auditory modality, prediction error is typically elicited using so-called oddball paradigms, where sequences of repeated pure tones with the same pitch are at unpredictable intervals substituted by a tone of deviant frequency. Repeated sounds become predictable promptly and elicit decreasing prediction error; deviant tones break these predictions and elicit large prediction errors. The simplicity of the rules inducing predictability make oddball paradigms agnostic about the origin of the predictions. Here, we introduce two possible models of the organizational topology of the predictive processing auditory network: (1) the global view, that assumes that predictions on the sensory input are generated at high-order levels of the cerebral cortex and transmitted in a cascade of generative models to the subcortical sensory pathways; and (2) the local view, that assumes that independent local models, computed using local information, are used to perform predictions at each processing stage. In the global view information encoding is optimized globally but biases sensory representations along the entire brain according to the subjective views of the observer. The local view results in a diminished coding efficiency, but guarantees in return a robust encoding of the features of sensory input at each processing stage. Although most experimental results to-date are ambiguous in this respect, recent evidence favors the global model

Cross-modal processing of voices and faces in developmental prosopagnosia and developmental phonagnosia

Conspecifics can be recognized from either the face or the voice alone. However, person identity information is rarely encountered in purely unimodal situations and there is increasing evidence that the face and voice interact in neurotypical identity processing. Conversely, developmental deficits have been observed that seem to be selective for face and voice recognition, developmental prosopagnosia and developmental phonagnosia, respectively. To date, studies on developmental prosopagnosia and phonagnosia have largely centred on within modality testing. Here, we review evidence from a small number of behavioural and neuroimaging studies which have examined the recognition of both faces and voices in these cohorts. A consensus from the findings is that, when tested in purely unimodal conditions, voice-identity processing appears normal in most cases of developmental prosopagnosia, as does face-identity processing in developmental phonagnosia. However, there is now first evidence that the multisensory nature of person identity impacts on identity recognition abilities in these cohorts. For example, unlike neurotypicals, auditory-only voice recognition is not enhanced in developmental prosopagnosia for voices which have been previously learned together with a face. This might also explain why the recognition of personally familiar voices is poorer in developmental prosopagnosics, compared to controls. In contrast, there is evidence that multisensory interactions might also lead to compensatory mechanisms in these disorders. For example, in developmental phonagnosia, voice recognition may be enhanced if voices have been learned with a corresponding face. Taken together, the reviewed findings challenge traditional models of person recognition which have assumed independence between face-identity and voice-identity processing and rather support an audio-visual model of human communication that assumes direction interactions between voice and face processing streams. In addition, the reviewed findings open up novel empirical research questions and have important implications for potential training regimes for developmental prosopagnosia and phonagnosia

Dorsal‐movement and ventral‐form regions are functionally connected during visual‐speech recognition

Faces convey social information such as emotion and speech. Facial emotion processing is supported via interactions between dorsal‐movement and ventral‐form visual cortex regions. Here, we explored, for the first time, whether similar dorsal–ventral interactions (assessed via functional connectivity), might also exist for visual‐speech processing. We then examined whether altered dorsal–ventral connectivity is observed in adults with high‐functioning autism spectrum disorder (ASD), a disorder associated with impaired visual‐speech recognition. We acquired functional magnetic resonance imaging (fMRI) data with concurrent eye tracking in pairwise matched control and ASD participants. In both groups, dorsal‐movement regions in the visual motion area 5 (V5/MT) and the temporal visual speech area (TVSA) were functionally connected to ventral‐form regions (i.e., the occipital face area [OFA] and the fusiform face area [FFA]) during the recognition of visual speech, in contrast to the recognition of face identity. Notably, parts of this functional connectivity were decreased in the ASD group compared to the controls (i.e., right V5/MT—right OFA, left TVSA—left FFA). The results confirmed our hypothesis that functional connectivity between dorsal‐movement and ventral‐form regions exists during visual‐speech processing. Its partial dysfunction in ASD might contribute to difficulties in the recognition of dynamic face information relevant for successful face‐to‐face communication

Altered processing of communication signals in the subcortical auditory sensory pathway in autism

Autism spectrum disorder (ASD) is characterised by social communication difficulties. These difficulties have been mainly explained by cognitive, motivational, and emotional alterations in ASD. The communication difficulties could, however, also be associated with altered sensory processing of communication signals. Here, we assessed the functional integrity of auditory sensory pathway nuclei in ASD in three independent functional magnetic resonance imaging experiments. We focused on two aspects of auditory communication that are impaired in ASD: voice identity perception, and recognising speech-in-noise. We found reduced processing in adults with ASD as compared to typically developed control groups (pairwise matched on sex, age, and full-scale IQ) in the central midbrain structure of the auditory pathway (inferior colliculus [IC]). The right IC responded less in the ASD as compared to the control group for voice identity, in contrast to speech recognition. The right IC also responded less in the ASD as compared to the control group when passively listening to vocal in contrast to non-vocal sounds. Within the control group, the left and right IC responded more when recognising speech-in-noise as compared to when recognising speech without additional noise. In the ASD group, this was only the case in the left, but not the right IC. The results show that communication signal processing in ASD is associated with reduced subcortical sensory functioning in the midbrain. The results highlight the importance of considering sensory processing alterations in explaining communication difficulties, which are at the core of ASD

Deficits in voice-identity processing: Acquired and developmental phonagnosia

The voice contains elementary social communication cues, conveying speech, as well as paralinguistic information pertaining to the emotional state and the identity of the speaker. In contrast to vocal-speech and vocal-emotion processing, voice-identity processing has been less explored. This seems surprising, given the day-to-day significance of person recognition by voice. A valuable approach to unravel how voice-identity processing is accomplished is to investigate people who have a selective deficit in recognising voices. Such a deficit has been termed phonagnosia. In the present chapter, we provide a systematic overview of studies on phonagnosia and how they relate to current neurocognitive models of person recognition. We review studies that have characterised people who suffer from phonagnosia following brain damage (i.e. acquired phonagnosia) and also studies, which have examined phonagnosia cases without apparent brain lesion (i.e. developmental phonagnosia). Based on the reviewed literature, we emphasise the need for a careful behavioural characterisation of phonagnosia cases by taking into consideration the multistage nature of voice-identity processing and the resulting behavioural phonagnosia subtypes

An information theoretic characterisation of auditory encoding.

The entropy metric derived from information theory provides a means to quantify the amount of information transmitted in acoustic streams like speech or music. By systematically varying the entropy of pitch sequences, we sought brain areas where neural activity and energetic demands increase as a function of entropy. Such a relationship is predicted to occur in an efficient encoding mechanism that uses less computational resource when less information is present in the signal: we specifically tested the hypothesis that such a relationship is present in the planum temporale (PT). In two convergent functional MRI studies, we demonstrated this relationship in PT for encoding, while furthermore showing that a distributed fronto-parietal network for retrieval of acoustic information is independent of entropy. The results establish PT as an efficient neural engine that demands less computational resource to encode redundant signals than those with high information content

Dysfunction of the visual sensory thalamus in developmental dyslexia

Developmental dyslexia (DD) is a reading disorder with a prevalence of 5-10%. Neuroscientific research has typically focused on explaining DD symptoms based on pathophysiological changes in the cerebral cortex. However, DD might also be associated with alterations in sensory thalami – central subcortical stations of sensory pathways. A post-mortem study on the visual sensory thalamus (lateral geniculate nucleus, LGN) showed histopathological changes in the magnocellular (M-LGN), but not in the parvocellular (P-LGN), subdivisions. M-LGN and P-LGN have different functional properties and belong to two different visual systems. Whether M-LGN alterations also exist in DD in-vivo is unclear. Also, the potential relevance of M-LGN alterations to DD symptoms is unknown. This lack of knowledge is partly due to considerable technical challenges in investigating LGN subdivisions non-invasively in humans. Here, we employed recent advances in high-field 7 Tesla functional magnetic resonance imaging (fMRI) to map the M- and P-LGN in-vivo in DD adults (n=26) and matched controls (n=28). We show that (i) M-LGN responses differ between DD and control participants, (ii) these differences are more pronounced in male than in female DD participants, and (iii) M-LGN alterations predict a core symptom of DD in male DD participants only, i.e., rapid naming ability. Our results provide a first functional interpretation of M-LGN changes in DD and support DD theories that propose a direct relevance of sensory thalamus alterations for DD symptoms. In addition, the sex-specific behavioral relevance of M-LGN alterations within DD calls for taking sex differences into account when planning brain-based therapeutic interventions