Divergent Human Cortical Regions for Processing Distinct Acoustic-Semantic Categories of Natural Sounds: Animal Action Sounds vs. Vocalizations

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.

Auditory object perception: A neurobiological model and prospective review

“…3, labeled yellow region) shows interaction or integration effects when corresponding sounds are also present (Calvert et al, 2000; Beauchamp et al, 2004b, 2004a; Taylor et al, 2006, 2009; Campanella and Belin, 2007; Campbell, 2008), and are generally activated by human action sounds in the absence of visual input (Lewis et al, 2004, 2006; Bidet-Caulet et al., 2005; Gazzola et al, 2006; Galati et al, 2008; Engel et al, 2009). These regions were further shown to be more strongly activated by human action sounds relative to non-human animal action sounds, and lesser still by non-living action sounds (Engel et al, 2009) or vocalizations (Webster et al, 2017). Thus, from a bottom-up signal processing perspective, these complexes appear to play a prominent perceptual role in transforming the spatially and temporally dynamic features of natural auditory (and visual) action information into a common neural code, conveying symbolic associations of physically matched audio-visual features.…”

“…A recent fMRI study by our group directly tested where auditory pathways for processing action sounds by living things versus vocalizations might diverge (Webster et al, 2017). Non-human animal vocalizations and non-human action sounds were used to minimize confounds associated with potentially greater semantic processing of conspecific sounds.…”

“…For instance, the left and right posterior insulae were more strongly activated by action sounds that were clearly perceived as being caused by an animal versus a human agent under different listening tasks or with different listening experiences, and were presumed to have functions related to audio-tactile or audio-sensorimotor associations (Engel et al, 2009; Lewis et al, 2011a; Webster et al, 2017). The human action sounds, relative to animal actions, more prominently activated a left-lateralized fronto-parietal and pSTS/pMTG network, overlapping mirror neuron systems (MNS), classically defined as involving the inferior parietal lobule, inferior frontal gyrus plus ventral premotor cortex (Rizzolatti and Craighero, 2004; Molenberghs et al, 2012).…”

“…Red colored cortices correspond to vocalizations, yellow to biological action sounds, and blue to non-living environmental and mechanical action sounds. Studies include selected results restricted to the defined sound category boundaries from Lewis et al, (2004, 2005, 2006, 2009); Engel et al (2009); Lewis et al (2011a), (2011b), (2012); and Webster et al (2017)). Refer to color key and text for other details.…”

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

“…This included three basic categories of soundsource: (1) action sounds (non-vocalizations) produced by ‘living things’, with human (conspecific) and non-human animal sources representing two subcategories; (2) action sounds produced by ‘nonliving things’, including environmental sounds and human-made machinery; and (3) vocalizations (‘living things’), with human versus nonhuman animals as two subcategories therein. This model was supported in a study that utilized non-human animal action sounds and vocalizations (also used in the present study), which minimized potential confounds related to the processing of deeper semantic encodings in meaning conveyed by commonly experienced (“over-learned”) human conspecific sounds (Webster et al, 2017). The goal of the present study was to determine if this same basic organizational principle, namely the processing along separable cortical pathways, might also be respected in some of the cortical regions involved in planning and orchestrating oral mimicry of these same sounds at a categorical level.…”