Auditory object perception: A neurobiological model and prospective review

Abstract

Interaction with the world is a multisensory experience, but most of what is known about the neural correlates of perception comes from studying vision. Auditory inputs enter cortex with its own set of unique qualities, and leads to use in oral communication, speech, music, and the understanding of emotional and intentional states of others, all of which are central to the human experience. To better understand how the auditory system develops, recovers after injury, and how it may have transitioned in its functions over the course of hominin evolution, advances are needed in models of how the human brain is organized to process real-world natural sounds and “auditory objects”. This review presents a simple fundamental neurobiological model of hearing perception at a category level that incorporates principles of bottom-up signal processing together with top-down constraints of grounded cognition theories of knowledge representation. Though mostly derived from human neuroimaging literature, this theoretical framework highlights rudimentary principles of real-world sound processing that may apply to most if not all mammalian species with hearing and acoustic communication abilities. The model encompasses three basic categories of sound-source: (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 ‘non-living things’, including environmental sources and human-made machinery; and (3) vocalizations (‘living things’), with human versus non-human animals as two subcategories therein. The model is presented in the context of cognitive architectures relating to multisensory, sensory-motor, and spoken language organizations. The models’ predictive values are further discussed in the context of anthropological theories of oral communication evolution and the neurodevelopment of spoken language proto-networks in infants/toddlers. These phylogenetic and ontogenetic frameworks both entail cortical network maturations that are proposed to at least in part be organized around a number of universal acoustic-semantic signal attributes of natural sounds, which are addressed herein.

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

“…The finding of a “double-dissociation” of oral mimicry networks, with consideration given to perceived mimicry difficulty and quality, was suggestive of separable neuronal architectures, and thus potentially separable cognitive processes (Shallice, 1988) related to aspects of auditory working memory, motor planning, and/or motor execution during oral mimicry at a categorical level. Importantly, these findings paralleled the dissociated cortical network organization reported in a recent neurobiological model of natural sound processing and perception (Brefczynski-Lewis and Lewis, 2017; Webster et al, 2017), which had been developed in part using some of the same ethologically validated, non-verbal sound stimuli. Because no overt speech or verbal processing was involved in either the task or stimuli, the present results may reflect cortical network vestiges underlying rudimentary elements of oral communication systems that are directly related to the statistics of physical attributes inherent to different semantic categories of real-world sound-producing events.…”

“…A neurobiological model of the organization of the human brain for processing and recognizing different acoustic-semantic categories of natural sounds [from Brefczynski-Lewis and Lewis (2017)]. Bold text in the boxed regions depict rudimentary sound categories proposed to represent ethologically relevant categories germane to sound recognition for all mammalian species.…”

“…From the perspective of hearing perception, we recently developed a neurobiological model for the processing of different acoustic-semantic categories of real-world natural sounds that may apply to all social mammals with hearing ability (Brefczynski-Lewis and Lewis, 2017): This model (Fig. 1) was based largely on neuroimaging results from both human adults (Belin, Zatorre, Lafaille, Ahad, & Pike, 2000; Clarke, Bellmann, de Ribaupierre, & Assal, 1996; Engel, Frum, Puce, Walker, & Lewis, 2009; Engelien et al, 2006; Lewis et al, 2009; Lewis, Brefczynski, Phinney, Janik, & DeYoe, 2005; Lewis, Talkington, Puce, Engel, & Frum, 2011; Lewis, Talkington, Tallaksen, & Frum, 2012; Webster et al, 2017) and infants (Geangu, Quadrelli, Lewis, Macchi Cassia, & Turati, 2015).…”

Agnosia for bird calls

“…This is attributable in part to a lack of detailed neuropsychological models of nonverbal auditory semantics and also the comparative rarity of reports of selective auditory agnosia, which might reveal the critical underlying cognitive architecture ( Engelien et al, 1995 , Clarke et al, 2000 , Hattiangadi et al, 2005 , Saygin et al, 2010 , Slevc and Shell, 2015 ). It has been proposed that the processing of sounds as ‘auditory objects’ may be organised analogously to visual object processing, with corresponding neural mechanisms in auditory cortex and its connections in the temporal, parietal and frontal lobes ( Goll et al, 2010a , Goll et al, 2010b , Brefczynski-Lewis and Lewis, 2017 ). However, opportunities to resolve key issues in auditory cognition – based on the study of patients with relevant deficits – remain limited.…”

Tinnitus: Una patología cerebral

“…Hasta este punto no podemos hablar de percepción, sino sólo de respuestas fisiológicas al estímulo acústico. Para que exista la percepción de un estímulo sonoro, es necesario que la actividad neuronal desencadenada a nivel de la corteza auditiva sea enviada a otros centros de procesamiento cerebral, las que además de la corteza auditiva incluyen a cortezas de procesamiento cognitivo, emocional, y de memoria entre otras 14 . La actividad de todas estas áreas en su conjunto, así como el nivel de comunicación entre ellas, es lo que genera la percepción auditiva.…”