Distinct Cortical Pathways for Processing Tool versus Animal Sounds

Abstract

Human listeners can effortlessly categorize a wide range of environmental sounds. Whereas categorizing visual object classes (e.g., faces, tools, houses, etc.) preferentially activates different regions of visually sensitive cortex, it is not known whether the auditory system exhibits a similar organization for different types or categories of complex sounds outside of human speech. Using functional magnetic resonance imaging, we show that hearing and correctly or incorrectly categorizing animal vocalizations (as opposed to handmanipulated tool sounds) preferentially activated middle portions of the left and right superior temporal gyri (mSTG). On average, the vocalization sounds had much greater harmonic and phase-coupling content (acoustically similar to human speech sounds), which may represent some of the signal attributes that preferentially activate the mSTG regions. In contrast, correctly categorized tool sounds (and even animal sounds that were miscategorized as being tool-related sounds) preferentially activated a widespread, predominantly left hemisphere cortical "mirror network." This network directly overlapped substantial portions of motor-related cortices that were independently activated when participants pantomimed tool manipulations with their right (dominant) hand. These data suggest that the recognition processing for some sounds involves a causal reasoning mechanism (a high-level auditory "how" pathway), automatically evoked when attending to hand-manipulated tool sounds, that effectively associates the dynamic motor actions likely to have produced the sound(s).

The functional role of the parieto-frontal mirror circuit: interpretations and misinterpretations

“…Hearing and categorizing animal vocalizations preferentially activated the middle portion of the superior temporal gyri bilaterally (a region that is not related to motor act coding), whereas hearing and categorizing sounds of tools that were manipulated by hands activated the parieto-frontal mirror circuit 53 . Similarly, it was shown that listening to the sound of hand and mouth motor acts activated the parieto-frontal mirror network 54 .…”

Repetition-Induced Plasticity of Motor Representations of Action Sounds

“…Apart from the well documented activations within auditory regions, environmental sounds related to actions were shown to co-activate parts of prefrontal, premotor and motor cortices bilaterally (Lahav et al 2007;De Lucia et al 2009) or predominantly on the left side (Lewis et al 2005;Pizzamiglio et al 2005;Gazzola et al 2006;Hauk et al 2006;Doehrmann et al 2008). The specific involvement of the primary motor cortex was demonstrated by transcranial magnetic stimulation (TMS); motor evoked potentials (MEPs) to stimulation of the hand area were shown to be larger while subjects listened to manualaction-related than unrelated sounds (Aziz-Zadeh et al 2004).…”

Familiarity affects environmental sound processing outside the focus of attention: An event-related potential study

“…Relevant significant interactions were specified by calculating reduced ANOVAs 2 Animal sounds are typically characterized by a high HNR in contrast to other types of environmental sounds, as e.g., household sounds (cf. Lewis et al, 2005). As a consequence of the applied stimulus manipulation, the HNR was lower for the unfamiliar than the familiar stimulus [1.22 vs. 6.05 dB (determined using default parameters with Praat, freely available phonetics software, http://www.fon.hum.uva.nl/praat/)].…”

“…To date, the processing of environmental sounds has mainly been studied when sounds were processed attentively (e.g., van Petten and Rheinfelder, 1995;Lewis et al, 2005;Cummings et al, 2006;Lenz et al, 2007;Murray et al, 2008). However, as familiar environmental sounds might convey behaviorally and biologically relevant information, processing advantages for familiar sounds might be expected even when sounds are processed outside the focus of attention.…”