A temporal hierarchy for conspecific vocalization discrimination in humans.
The ability to discriminate conspecific vocalizations is observed across species and early during development. However, its neurophysiologic mechanism remains controversial, particularly regarding whether it involves specialized processes with dedicated neural machinery. We identified spatiotemporal brain mechanisms for conspecific vocalization discrimination in humans by applying electrical neuroimaging analyses to auditory evoked potentials (AEPs) in response to acoustically and psychophysically controlled nonverbal human and animal vocalizations as well as sounds of man-made objects. AEP strength modulations in the absence of topographic modulations are suggestive of statistically indistinguishable brain networks. First, responses were significantly stronger, but topographically indistinguishable to human versus animal vocalizations starting at 169-219 ms after stimulus onset and within regions of the right superior temporal sulcus and superior temporal gyrus. This effect correlated with another AEP strength modulation occurring at 291-357 ms that was localized within the left inferior prefrontal and precentral gyri. Temporally segregated and spatially distributed stages of vocalization discrimination are thus functionally coupled and demonstrate how conventional views of functional specialization must incorporate network dynamics. Second, vocalization discrimination is not subject to facilitated processing in time, but instead lags more general categorization by approximately 100 ms, indicative of hierarchical processing during object discrimination. Third, although differences between human and animal vocalizations persisted when analyses were performed at a single-object level or extended to include additional (man-made) sound categories, at no latency were responses to human vocalizations stronger than those to all other categories. Vocalization discrimination transpires at times synchronous with that of face discrimination but is not functionally specialized.
De Lucia
Marzia
M
Electroencephalography Brain Mapping Core, Center for Biomedical Imaging, Vaudois University Hospital Center and University of Lausanne, 1011 Lausanne, Switzerland.
Clarke
Stephanie
S
Murray
Micah M
MM
D000161:Acoustic Stimulation; D000328:Adult; D000818:Animals; D001307:Auditory Perception / Q000502:physiology*; D001921:Brain / Q000502:physiology*; D001931:Brain Mapping; D004192:Discrimination, Psychological / Q000502:physiology*; D004569:Electroencephalography; D005072:Evoked Potentials, Auditory; D005260:Female; D006801:Humans; D008297:Male; D009434:Neural Pathways / Q000502:physiology; D009483:Neuropsychological Tests; D013018:Sound Spectrography; D013045:Species Specificity; D013060:Speech; D013067:Speech Perception / Q000502:physiology*; D013997:Time Factors; D014828:Vocalization, Animal; D055815:Young Adult