Processing of Natural Sounds in Human Auditory Cortex: Tonotopy, Spectral Tuning, and Relation to Voice Sensitivity

Abstract

Auditory cortical processing of complex meaningful sounds entails the transformation of sensory (tonotopic) representations of incoming acoustic waveforms into higher-level sound representations (e.g., their category). However, the precise neural mechanisms enabling such transformations remain largely unknown. In the present study, we use functional magnetic resonance imaging (fMRI) and natural sounds stimulation to examine these two levels of sound representation (and their relation) in the human auditory cortex. In a first experiment, we derive cortical maps of frequency preference (tonotopy) and selectivity (tuning width) by mathematical modeling of fMRI responses to natural sounds. The tuning width maps highlight a region of narrow tuning that follows the main axis of Heschl's gyrus and is flanked by regions of broader tuning. The narrowly tuned portion on Heschl's gyrus contains two mirror-symmetric frequency gradients, presumably defining two distinct primary auditory areas. In addition, our analysis indicates that spectral preference and selectivity (and their topographical organization) extend well beyond the primary regions and also cover higher-order and categoryselective auditory regions. In particular, regions with preferential responses to human voice and speech occupy the low-frequency portions of the tonotopic map. We confirm this observation in a second experiment, where we find that speech/voice selective regions exhibit a response bias toward the low frequencies characteristic of human voice and speech, even when responding to simple tones. We propose that this frequency bias reflects the selective amplification of relevant and category-characteristic spectral bands, a useful processing step for transforming a sensory (tonotopic) sound image into higher level neural representations.

Tonotopic maps in human auditory cortex using arterial spin labeling

“…S6 and S7). This configuration is in agreement with previous studies, although an additional cluster on anterior STS in the right hemisphere is sometimes found (Belin et al, 2000; Bonte et al, 2013, 2014; Moerel et al, 2012; Pernet et al, 2015). In contrast, the extension of CBF voice selective regions was very limited, probably due to the lower CNR as suggested by below‐threshold effects (see Supporting Information Fig.…”

“…The overall layout and the spatial arrangement of the tonotopic gradients described for the CBF tonotopy is in good (qualitative) agreement with those in the BOLD tonotopy (in the corresponding panel of Fig. 3A, the two reversed gradients forming the high‐low‐high frequency pattern are indicated by white double arrows and the additional low frequency clusters by black single arrows), and similar to maps shown in previously published BOLD signal studies (Da Costa et al, 2011; Formisano et al, 2003; Humphries et al, 2010; Moerel et al, 2012). However, in the CBF tonotopy, extreme low or high preferred frequency values are less represented than in the BOLD tonotopy.…”

“…For visualization, the maps were projected on the inflated cortical surfaces. The color‐coded single‐subject maps were transformed into the common CBA space and averaged to obtain a group tonotopic map (Da Costa et al, 2011; De Martino et al, 2013; Formisano et al, 2003; Herdener et al, 2013; Humphries et al, 2010; Langers et al, 2007; Moerel et al, 2012). …”

Areas activated during naturalistic reading comprehension overlap topological visual, auditory, and somatotomotor maps

“…Our results are consistent with these findings. Our results also confirm a previous finding that the tonotopic maps overlapping reading activation in the STG have a bias toward the lower frequencies [Moerel et al, 2012], a range occupied by human voices.…”

“…It has been reported previously that tonotopic maps in auditory cortex overlap with temporal voice areas [Belin et al, 2000] in STG [Moerel et al, 2012]. Additionally, silent active reading has been shown to activate temporal voice areas [Perrone‐Bertolotti et al, 2012].…”