Receptive prosody in nonfluent primary progressive aphasias.

INTRODUCTION: Prosody has been little studied in the primary progressive aphasias (PPAs), a group of neurodegenerative disorders presenting with progressive language impairment. METHODS: Here we conducted a systematic investigation of different dimensions of prosody processing (acoustic, linguistic and emotional) in a cohort of 19 patients with nonfluent PPA syndromes (11 with progressive nonfluent aphasia, PNFA; five with progressive logopenic/phonological aphasia, LPA; three with progranulin-associated aphasia, GRN-PPA) compared with a group of healthy older controls. Voxel-based morphometry (VBM) was used to identify neuroanatomical associations of prosodic functions. RESULTS: Broadly comparable receptive prosodic deficits were exhibited by the PNFA, LPA and GRN-PPA subgroups, for acoustic, linguistic and affective dimensions of prosodic analysis. Discrimination of prosodic contours was significantly more impaired than discrimination of simple acoustic cues, and discrimination of intonation was significantly more impaired than discrimination of stress at phrasal level. Recognition of vocal emotions was more impaired than recognition of facial expressions for the PPA cohort, and recognition of certain emotions (in particular, disgust and fear) was relatively more impaired than others (sadness, surprise). VBM revealed atrophy associated with acoustic and linguistic prosody impairments in a distributed cortical network including areas likely to be involved in perceptual analysis of vocalisations (posterior temporal and inferior parietal cortices) and working memory (fronto-parietal circuitry). Grey matter associations of emotional prosody processing were identified for negative emotions (disgust, fear, sadness) in a broadly overlapping network of frontal, temporal, limbic and parietal areas. CONCLUSIONS: Taken together, the findings show that receptive prosody is impaired in nonfluent PPA syndromes, and suggest a generic early perceptual deficit of prosodic signal analysis with additional relatively specific deficits (recognition of particular vocal emotions).

Early specialization for voice and emotion processing in the infant brain.

Human voices play a fundamental role in social communication, and areas of the adult "social brain" show specialization for processing voices and their emotional content (superior temporal sulcus, inferior prefrontal cortex, premotor cortical regions, amygdala, and insula). However, it is unclear when this specialization develops. Functional magnetic resonance (fMRI) studies suggest that the infant temporal cortex does not differentiate speech from music or backward speech, but a prior study with functional near-infrared spectroscopy revealed preferential activation for human voices in 7-month-olds, in a more posterior location of the temporal cortex than in adults. However, the brain networks involved in processing nonspeech human vocalizations in early development are still unknown. To address this issue, in the present fMRI study, 3- to 7-month-olds were presented with adult nonspeech vocalizations (emotionally neutral, emotionally positive, and emotionally negative) and nonvocal environmental sounds. Infants displayed significant differential activation in the anterior portion of the temporal cortex, similarly to adults. Moreover, sad vocalizations modulated the activity of brain regions involved in processing affective stimuli such as the orbitofrontal cortex and insula. These results suggest remarkably early functional specialization for processing human voice and negative emotions.

Suppressing sensorimotor activity modulates the discrimination of auditory emotions but not speaker identity.

Our ability to recognize the emotions of others is a crucial feature of human social cognition. Functional neuroimaging studies indicate that activity in sensorimotor cortices is evoked during the perception of emotion. In the visual domain, right somatosensory cortex activity has been shown to be critical for facial emotion recognition. However, the importance of sensorimotor representations in modalities outside of vision remains unknown. Here we use continuous theta-burst transcranial magnetic stimulation (cTBS) to investigate whether neural activity in the right postcentral gyrus (rPoG) and right lateral premotor cortex (rPM) is involved in nonverbal auditory emotion recognition. Three groups of participants completed same-different tasks on auditory stimuli, discriminating between the emotion expressed and the speakers' identities, before and following cTBS targeted at rPoG, rPM, or the vertex (control site). A task-selective deficit in auditory emotion discrimination was observed. Stimulation to rPoG and rPM resulted in a disruption of participants' abilities to discriminate emotion, but not identity, from vocal signals. These findings suggest that sensorimotor activity may be a modality-independent mechanism which aids emotion discrimination.

Developmental phonagnosia: a selective deficit of vocal identity recognition.

Phonagnosia, the inability to recognize familiar voices, has been studied in brain-damaged patients but no cases due to developmental problems have been reported. Here we describe the case of KH, a 60-year-old active professional woman who reports that she has always experienced severe voice recognition difficulties. Her hearing abilities are normal, and an MRI scan showed no evidence of brain damage in regions associated with voice or auditory perception. To better understand her condition and to assess models of voice and high-level auditory processing, we tested KH on behavioural tasks measuring voice recognition, recognition of vocal emotions, face recognition, speech perception, and processing of environmental sounds and music. KH was impaired on tasks requiring the recognition of famous voices and the learning and recognition of new voices. In contrast, she performed well on nearly all other tasks. Her case is the first report of developmental phonagnosia, and the results suggest that the recognition of a speaker's vocal identity depends on separable mechanisms from those used to recognize other information from the voice or non-vocal auditory stimuli.

Positive emotions preferentially engage an auditory-motor "mirror" system.

Social interaction relies on the ability to react to communication signals. Although cortical sensory-motor "mirror" networks are thought to play a key role in visual aspects of primate communication, evidence for a similar generic role for auditory-motor interaction in primate nonverbal communication is lacking. We demonstrate that a network of human premotor cortical regions activated during facial movement is also involved in auditory processing of affective nonverbal vocalizations. Within this auditory-motor mirror network, distinct functional subsystems respond preferentially to emotional valence and arousal properties of heard vocalizations. Positive emotional valence enhanced activation in a left posterior inferior frontal region involved in representation of prototypic actions, whereas increasing arousal enhanced activation in presupplementary motor area cortex involved in higher-order motor control. Our findings demonstrate that listening to nonverbal vocalizations can automatically engage preparation of responsive orofacial gestures, an effect that is greatest for positive-valence and high-arousal emotions. The automatic engagement of responsive orofacial gestures by emotional vocalizations suggests that auditory-motor interactions provide a fundamental mechanism for mirroring the emotional states of others during primate social behavior. Motor facilitation by positive vocal emotions suggests a basic neural mechanism for establishing cohesive bonds within primate social groups.