Electrophysiological Evidence of Early Cortical Sensitivity to Human Conspecific Mimic Voice as a Distinct Category of Natural Sound.

Purpose From an anthropological perspective of hominin communication, the human auditory system likely evolved to enable special sensitivity to sounds produced by the vocal tracts of human conspecifics whether attended or passively heard. While numerous electrophysiological studies have used stereotypical human-produced verbal (speech voice and singing voice) and nonverbal vocalizations to identify human voice-sensitive responses, controversy remains as to when (and where) processing of acoustic signal attributes characteristic of "human voiceness" per se initiate in the brain. Method To explore this, we used animal vocalizations and human-mimicked versions of those calls ("mimic voice") to examine late auditory evoked potential responses in humans. Results Here, we revealed an N1b component (96-120 ms poststimulus) during a nonattending listening condition showing significantly greater magnitude in response to mimics, beginning as early as primary auditory cortices, preceding the time window reported in previous studies that revealed species-specific vocalization processing initiating in the range of 147-219 ms. During a sound discrimination task, a P600 (500-700 ms poststimulus) component showed specificity for accurate discrimination of human mimic voice. Distinct acoustic signal attributes and features of the stimuli were used in a classifier model, which could distinguish most human from animal voice comparably to behavioral data-though none of these single features could adequately distinguish human voiceness. Conclusions These results provide novel ideas for algorithms used in neuromimetic hearing aids, as well as direct electrophysiological support for a neurocognitive model of natural sound processing that informs both neurodevelopmental and anthropological models regarding the establishment of auditory communication systems in humans. Supplemental Material https://doi.org/10.23641/asha.12903839.

Processing of Real-World, Dynamic Natural Stimuli in Autism is Linked to Corticobasal Function.

Many individuals with autism spectrum disorder (ASD) have been shown to perceive everyday sensory information differently compared to peers without autism. Research examining these sensory differences has primarily utilized nonnatural stimuli or natural stimuli using static photos with few having utilized dynamic, real-world nonverbal stimuli. Therefore, in this study, we used functional magnetic resonance imaging to characterize brain activation of individuals with high-functioning autism when viewing and listening to a video of a real-world scene (a person bouncing a ball) and anticipating the bounce. We investigated both multisensory and unisensory processing and hypothesized that individuals with ASD would show differential activation in (a) primary auditory and visual sensory cortical and association areas, and in (b) cortical and subcortical regions where auditory and visual information is integrated (e.g. temporal-parietal junction, pulvinar, superior colliculus). Contrary to our hypotheses, the whole-brain analysis revealed similar activation between the groups in these brain regions. However, compared to controls the ASD group showed significant hypoactivation in the left intraparietal sulcus and left putamen/globus pallidus. We theorize that this hypoactivation reflected underconnectivity for mediating spatiotemporal processing of the visual biological motion stimuli with the task demands of anticipating the timing of the bounce event. The paradigm thus may have tapped into a specific left-lateralized aberrant corticobasal circuit or loop involved in initiating or inhibiting motor responses. This was consistent with a dual "when versus where" psychophysical model of corticobasal function, which may reflect core differences in sensory processing of real-world, nonverbal natural stimuli in ASD. Autism Res 2020, 13: 539-549. © 2020 International Society for Autism Research, Wiley Periodicals, Inc. LAY SUMMARY: To understand how individuals with autism perceive the real-world, using magnetic resonance imaging we examined brain activation in individuals with autism while watching a video of someone bouncing a basketball. Those with autism had similar activation to controls in auditory and visual sensory brain regions, but less activation in an area that processes information about body movements and in a region involved in modulating movements. These areas are important for understanding the actions of others and developing social skills.

Hearing and orally mimicking different acoustic-semantic categories of natural sound engage distinct left hemisphere cortical regions.

Oral mimicry is thought to represent an essential process for the neurodevelopment of spoken language systems in infants, the evolution of language in hominins, and a process that could possibly aid recovery in stroke patients. Using functional magnetic resonance imaging (fMRI), we previously reported a divergence of auditory cortical pathways mediating perception of specific categories of natural sounds. However, it remained unclear if or how this fundamental sensory organization by the brain might relate to motor output, such as sound mimicry. Here, using fMRI, we revealed a dissociation of activated brain regions preferential for hearing with the intent to imitate and the oral mimicry of animal action sounds versus animal vocalizations as distinct acoustic-semantic categories. This functional dissociation may reflect components of a rudimentary cortical architecture that links systems for processing acoustic-semantic universals of natural sound with motor-related systems mediating oral mimicry at a category level. The observation of different brain regions involved in different aspects of oral mimicry may inform targeted therapies for rehabilitation of functional abilities after stroke.

Cortical networks representing object categories and high-level attributes of familiar real-world action sounds.

In contrast to visual object processing, relatively little is known about how the human brain processes everyday real-world sounds, transforming highly complex acoustic signals into representations of meaningful events or auditory objects. We recently reported a fourfold cortical dissociation for representing action (nonvocalization) sounds correctly categorized as having been produced by human, animal, mechanical, or environmental sources. However, it was unclear how consistent those network representations were across individuals, given potential differences between each participant's degree of familiarity with the studied sounds. Moreover, it was unclear what, if any, auditory perceptual attributes might further distinguish the four conceptual sound-source categories, potentially revealing what might drive the cortical network organization for representing acoustic knowledge. Here, we used functional magnetic resonance imaging to test participants before and after extensive listening experience with action sounds, and tested for cortices that might be sensitive to each of three different high-level perceptual attributes relating to how a listener associates or interacts with the sound source. These included the sound's perceived concreteness, effectuality (ability to be affected by the listener), and spatial scale. Despite some variation of networks for environmental sounds, our results verified the stability of a fourfold dissociation of category-specific networks for real-world action sounds both before and after familiarity training. Additionally, we identified cortical regions parametrically modulated by each of the three high-level perceptual sound attributes. We propose that these attributes contribute to the network-level encoding of category-specific acoustic knowledge representations.

Different categories of living and non-living sound-sources activate distinct cortical networks.

With regard to hearing perception, it remains unclear as to whether, or the extent to which, different conceptual categories of real-world sounds and related categorical knowledge are differentially represented in the brain. Semantic knowledge representations are reported to include the major divisions of living versus non-living things, plus more specific categories including animals, tools, biological motion, faces, and places-categories typically defined by their characteristic visual features. Here, we used functional magnetic resonance imaging (fMRI) to identify brain regions showing preferential activity to four categories of action sounds, which included non-vocal human and animal actions (living), plus mechanical and environmental sound-producing actions (non-living). The results showed a striking antero-posterior division in cortical representations for sounds produced by living versus non-living sources. Additionally, there were several significant differences by category, depending on whether the task was category-specific (e.g. human or not) versus non-specific (detect end-of-sound). In general, (1) human-produced sounds yielded robust activation in the bilateral posterior superior temporal sulci independent of task. Task demands modulated activation of left lateralized fronto-parietal regions, bilateral insular cortices, and sub-cortical regions previously implicated in observation-execution matching, consistent with "embodied" and mirror-neuron network representations subserving recognition. (2) Animal action sounds preferentially activated the bilateral posterior insulae. (3) Mechanical sounds activated the anterior superior temporal gyri and parahippocampal cortices. (4) Environmental sounds preferentially activated dorsal occipital and medial parietal cortices. Overall, this multi-level dissociation of networks for preferentially representing distinct sound-source categories provides novel support for grounded cognition models that may underlie organizational principles for hearing perception.

Human cortical organization for processing vocalizations indicates representation of harmonic structure as a signal attribute.

The ability to detect and rapidly process harmonic sounds, which in nature are typical of animal vocalizations and speech, can be critical for communication among conspecifics and for survival. Single-unit studies have reported neurons in auditory cortex sensitive to specific combinations of frequencies (e.g., harmonics), theorized to rapidly abstract or filter for specific structures of incoming sounds, where large ensembles of such neurons may constitute spectral templates. We studied the contribution of harmonic structure to activation of putative spectral templates in human auditory cortex by using a wide variety of animal vocalizations, as well as artificially constructed iterated rippled noises (IRNs). Both the IRNs and vocalization sounds were quantitatively characterized by calculating a global harmonics-to-noise ratio (HNR). Using functional MRI, we identified HNR-sensitive regions when presenting either artificial IRNs and/or recordings of natural animal vocalizations. This activation included regions situated between functionally defined primary auditory cortices and regions preferential for processing human nonverbal vocalizations or speech sounds. These results demonstrate that the HNR of sound reflects an important second-order acoustic signal attribute that parametrically activates distinct pathways of human auditory cortex. Thus, these results provide novel support for the presence of spectral templates, which may subserve a major role in the hierarchical processing of vocalizations as a distinct category of behaviorally relevant sound.