Abstract
A major gap in our understanding of natural sound processing is knowledge of where or how in a cortical hierarchy differential processing leads to categorical perception at a semantic level. Here, using functional magnetic resonance imaging (fMRI) we sought to determine if and where cortical pathways in humans might diverge for processing action sounds vs. vocalizations as distinct acoustic-semantic categories of real-world sound when matched for duration and intensity. This was tested by using relatively less semantically complex natural sounds produced by non-conspecific animals rather than humans. Our results revealed a striking double-dissociation of activated networks bilaterally. This included a previously well described pathway preferential for processing vocalization signals directed laterally from functionally defined primary auditory cortices to the anterior superior temporal gyri, and a less well-described pathway preferential for processing animal action sounds directed medially to the posterior insulae. We additionally found that some of these regions and associated cortical networks showed parametric sensitivity to high-order quantifiable acoustic signal attributes and/or to perceptual features of the natural stimuli, such as the degree of perceived recognition or intentional understanding. Overall, these results supported a neurobiological theoretical framework for how the mammalian brain may be fundamentally organized to process acoustically and acoustic-semantically distinct categories of ethologically valid, real-world sounds.
Highlights
Critical to survival and social organization is our ability to view, hear, and understand the goals and intentions of others, including both human and non-human animals
The goal of the present study, using functional magnetic resonance imaging (fMRI), was to test for the existence of divergent cortical processing streams along human auditory cortices, presumably in both hemispheres, that respect the theorized acoustic-semantic boundary for processing non-conspecific animal action sounds vs. vocalizations as ideal stimulus sets to critically test this putative major boundary— which may represent a sensory processing boundary common to most if not all mammals
Contrasting brain activation preferential for one vs. the other semantic category of sound source revealed a robust double-dissociation of cortical regions showing significant preference for processing animal action sounds medially in the posterior insulae [Table 2 and Figure 2, solid yellow at p(uncorr) < 0.001, corrected to p(corr) < 0.05 for minimum cluster size, and transparent yellow at p(uncorr) < 0.01, p(corr) < 0.05] vs. processing of animal vocalizations laterally in the middle and anterior superior temporal gyri (STG) [red; p(uncorr) < 0.001, p(corr) < 0.05]
Summary
Critical to survival and social organization is our ability to view, hear, and understand the goals and intentions of others, including both human (conspecifics) and non-human (non-conspecific) animals It remains unclear how the human auditory system is fundamentally organized to process the diverse range of natural, biologically relevant sounds, such as speech and action events, and provide the listener with a sense of meaning. Ventrally directed cortical pathways, relative to PAC, are involved more in identification of sound patterns for perception of what the source is or its potential communicative content This dorsal vs ventral dichotomy has been applied to models of spoken language processing (MacNeilage, 1998; Rauschecker and Scott, 2009; Arbib, 2010; Perlovsky, 2011; DeWitt and Rauschecker, 2013). While hypothesized dorsal-ventral organizations for sound processing are reasonably well established, many gaps remain in our understanding of how the putative ventral pathways for sound recognition (“what is it”) may be organized to process the acoustic signal attributes that may be characteristic of different semantic or “acoustic-semantic” categories of natural sounds
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