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 (nonliving). 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 nonspecific (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 subcortical regions previously implicated in observation-execution matching, consistent with "embodied" and mirrorneuron 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.
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.
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