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

Abstract

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.

Bilateral reorganization of posterior temporal cortices in post‐lingual deafness and its relation to cochlear implant outcome

“…2, yellow blobs and Table III), who performed the task recruiting only the left inferior and superior frontal gyri and the bilateral cerebellum. Notably, they recruited none of the brain regions usually involved in environmental sound acoustic analysis and representation (i.e., the left parietal lobule and the right posterior temporal cortex) [Engel et al, 2009;Kraut et al, 2006;Lewis et al, 2004]. No activation during sound relative to color imagery in the CI candidate group was observed.…”

Evolution of non-speech sound memory in postlingual deafness: Implications for cochlear implant rehabilitation

“…We offer the hypothesis that this change occurred early in the time course of auditory deprivation for the right posterior temporal cortex, because its activation correlated with the duration of hearing loss rather than with the duration of deafness. Because the right posterior temporal cortex is specialized in multimodal integration of NSS and music (Beauchamp et al, 2004;Doehrmann & Naumer, 2008;Engel et al, 2009;Lewis et al, 2004;Zatorre & Halpern, 1993), when auditory inputs weaken and oral communication becomes cognitively more demanding, the involvement of the right posterior temporal cortex in NSS processing may decrease. This loss of function could potentially make available cognitive resources for phonological processing, as suggested by the observation that this region is abnormally recruited in post-lingual deaf subjects during phonological tasks (Lazard et al, 2010) or during lip reading (Lee, Truy, et al, 2007).…”

“…Sound imagery in normal-hearing subjects activated multimodal cognitive areas, the bilateral frontal and left parietotemporal areas (Kraut et al, 2006;Leff et al, 2008;Scott, Blank, Rosen, & Wise, 2000;Shannon & Buckner, 2004), and areas dedicated to NSS processing such as the right posterior temporal cortex and the left insula (Beauchamp, Lee, Argall, & Martin, 2004; Doehrmann & Naumer, 2008;Engel, Frum, Puce, Walker, & Lewis, 2009;Halpern & Zatorre, 1999;Lewis et al, 2004;Thierry et al, 2003;Zatorre & Halpern, 1993) (Fig. 2, grey blobs and Table 2).…”

Roaring lions and chirruping lemurs: How the brain encodes sound objects in space

“…The selectivity of the ventral stream for the meaning of sounds has been confirmed in a series of studies using different categories of environmental sounds as stimuli (e.g., tools, animals, man-made objects, living and non-living sound sources, actions, and musical instruments; Lewis et al 2005;Murray et al 2006;Altmann et al 2007;Engel et al 2009;Leaver and Rauschecker 2010;Lewis et al 2011). The processing which leads eventually to sound recognition involves two sequential steps, which are hierarchically organized.…”