A population of neurons selective for human voice in the monkey brain.

Many animals can extract useful information from the vocalizations of other species. Neuroimaging studies have evidenced areas sensitive to conspecific vocalizations in the cerebral cortex of primates, but how these areas process heterospecific vocalizations remains unclear. Using fMRI-guided electrophysiology, we recorded the spiking activity of individual neurons in the anterior temporal voice patches of two macaques while they listened to complex sounds including vocalizations from several species. In addition to cells selective for conspecific macaque vocalizations, we identified an unsuspected subpopulation of neurons with strong selectivity for human voice, not merely explained by spectral or temporal structure of the sounds. The auditory representational geometry implemented by these neurons was strongly related to that measured in the human voice areas with neuroimaging and only weakly to low-level acoustical structure. These findings provide new insights into the neural mechanisms involved in auditory expertise and the evolution of communication systems in primates.

The Encoding of Sound Source Elevation in the Human Auditory Cortex.

Spatial hearing is a crucial capacity of the auditory system. While the encoding of horizontal sound direction has been extensively studied, very little is known about the representation of vertical sound direction in the auditory cortex. Using high-resolution fMRI, we measured voxelwise sound elevation tuning curves in human auditory cortex and show that sound elevation is represented by broad tuning functions preferring lower elevations as well as secondary narrow tuning functions preferring individual elevation directions. We changed the ear shape of participants (male and female) with silicone molds for several days. This manipulation reduced or abolished the ability to discriminate sound elevation and flattened cortical tuning curves. Tuning curves recovered their original shape as participants adapted to the modified ears and regained elevation perception over time. These findings suggest that the elevation tuning observed in low-level auditory cortex did not arise from the physical features of the stimuli but is contingent on experience with spectral cues and covaries with the change in perception. One explanation for this observation may be that the tuning in low-level auditory cortex underlies the subjective perception of sound elevation.SIGNIFICANCE STATEMENT This study addresses two fundamental questions about the brain representation of sensory stimuli: how the vertical spatial axis of auditory space is represented in the auditory cortex and whether low-level sensory cortex represents physical stimulus features or subjective perceptual attributes. Using high-resolution fMRI, we show that vertical sound direction is represented by broad tuning functions preferring lower elevations as well as secondary narrow tuning functions preferring individual elevation directions. In addition, we demonstrate that the shape of these tuning functions is contingent on experience with spectral cues and covaries with the change in perception, which may indicate that the tuning functions in low-level auditory cortex underlie the perceived elevation of a sound source.

Perceptual grouping in the cocktail party: Contributions of voice-feature continuity.

Cocktail parties pose a difficult yet solvable problem for the auditory system. Previous work has shown that the cocktail-party problem is considerably easier when all sounds in the target stream are spoken by the same talker (the voice-continuity benefit). The present study investigated the contributions of two of the most salient voice features-glottal-pulse rate (GPR) and vocal-tract length (VTL)-to the voice-continuity benefit. Twenty young, normal-hearing listeners participated in two experiments. On each trial, listeners heard concurrent sequences of spoken digits from three different spatial locations and reported the digits coming from a target location. Critically, across conditions, GPR and VTL either remained constant or varied across target digits. Additionally, across experiments, the target location either remained constant (Experiment 1) or varied (Experiment 2) within a trial. In Experiment 1, listeners benefited from continuity in either voice feature, but VTL continuity was more helpful than GPR continuity. In Experiment 2, spatial discontinuity greatly hindered listeners' abilities to exploit continuity in GPR and VTL. The present results suggest that selective attention benefits from continuity in target voice features and that VTL and GPR play different roles for perceptual grouping and stream segregation in the cocktail party.

Fast and persistent adaptation to new spectral cues for sound localization suggests a many-to-one mapping mechanism.

The adult human auditory system can adapt to changes in spectral cues for sound localization. This plasticity was demonstrated by changing the shape of the pinna with earmolds. Previous results indicate that participants regain localization accuracy after several weeks of adaptation and that the adapted state is retained for at least one week without earmolds. No aftereffect was observed after mold removal, but any aftereffect may be too short to be observed when responses are averaged over many trials. This work investigated the lack of aftereffect by analyzing single-trial responses and modifying visual, auditory, and tactile information during the localization task. Results showed that participants localized accurately immediately after mold removal, even at the first stimulus presentation. Knowledge of the stimulus spectrum, tactile information about the absence of the earmolds, and visual feedback were not necessary to localize accurately after adaptation. Part of the adaptation persisted for one month without molds. The results are consistent with the hypothesis of a many-to-one mapping of the spectral cues, in which several spectral profiles are simultaneously associated with one sound location. Additionally, participants with acoustically more informative spectral cues localized sounds more accurately, and larger acoustical disturbances by the molds reduced adaptation success.

Adaptation to shifted interaural time differences changes encoding of sound location in human auditory cortex.

The auditory system infers the location of sound sources from the processing of different acoustic cues. These cues change during development and when assistive hearing devices are worn. Previous studies have found behavioral recalibration to modified localization cues in human adults, but very little is known about the neural correlates and mechanisms of this plasticity. We equipped participants with digital devices, worn in the ear canal that allowed us to delay sound input to one ear, and thus modify interaural time differences, a major cue for horizontal sound localization. Participants wore the digital earplugs continuously for nine days while engaged in day-to-day activities. Daily psychoacoustical testing showed rapid recalibration to the manipulation and confirmed that adults can adapt to shifted interaural time differences in their daily multisensory environment. High-resolution functional MRI scans performed before and after recalibration showed that recalibration was accompanied by changes in hemispheric lateralization of auditory cortex activity. These changes corresponded to a shift in spatial coding of sound direction comparable to the observed behavioral recalibration. Fitting the imaging results with a model of auditory spatial processing also revealed small shifts in voxel-wise spatial tuning within each hemisphere.

A small, but vocal, brain.

In the May issue of Cell Reports, Jafari et al.1 used ultra-high-field fMRI to show that marmosets, like humans and macaques, possess an extensive network of voice-selective areas.

The Temporal Voice Areas are not "just" Speech Areas.

The Temporal Voice Areas (TVAs) respond more strongly to speech sounds than to non-speech vocal sounds, but does this make them Temporal "Speech" Areas? We provide a perspective on this issue by combining univariate, multivariate, and representational similarity analyses of fMRI activations to a balanced set of speech and non-speech vocal sounds. We find that while speech sounds activate the TVAs more than non-speech vocal sounds, which is likely related to their larger temporal modulations in syllabic rate, they do not appear to activate additional areas nor are they segregated from the non-speech vocal sounds when their higher activation is controlled. It seems safe, then, to continue calling these regions the Temporal Voice Areas.

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 largely unknown. While primary auditory cortex is organized largely similarly in humans and macaques,1 the picture is much less clear at higher levels of the anterior auditory pathway,2 particularly regarding the processing of conspecific vocalizations (CVs). A "voice region" similar to the human voice-selective areas3,4 has been identified in the macaque right anterior temporal lobe with functional MRI;5 however, its anatomical localization, seemingly inconsistent with that of the human temporal voice areas (TVAs), has suggested a "repositioning of the voice area" in recent human evolution.6 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 possesses cortical voice areas that are bilateral and 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.

End level bias on direct loudness ratings of increasing sounds.

Three experiments on loudness of sounds with linearly increasing levels were performed: global loudness was measured using direct ratings, loudness change was measured using direct and indirect estimations. Results revealed differences between direct and indirect estimations of loudness change, indicating that the underlying perceptual phenomena are not the same. The effect of ramp size is small for the former and important for the latter. A similar trend was revealed between global loudness and direct estimations of loudness change according to the end level, suggesting they may have been confounded. Measures provided by direct estimations of loudness change are more participant-dependent.