Abstract

Little is known about how neural representations of natural sounds differ across species. For example, speech and music play a unique role in human hearing, yet it is unclear how auditory representations of speech and music differ between humans and other animals. Using functional ultrasound imaging, we measured responses in ferrets to a set of natural and spectrotemporally matched synthetic sounds previously tested in humans. Ferrets showed similar lower-level frequency and modulation tuning to that observed in humans. But while humans showed substantially larger responses to natural vs. synthetic speech and music in non-primary regions, ferret responses to natural and synthetic sounds were closely matched throughout primary and non-primary auditory cortex, even when tested with ferret vocalizations. This finding reveals that auditory representations in humans and ferrets diverge sharply at late stages of cortical processing, potentially driven by higher-order processing demands in speech and music.

Highlights

  • Little is known about how sensory representations of natural stimuli differ across species (Theunissen and Elie, 2014)

  • We test three key hypotheses: (1) higher-o­ rder sensitivity in humans reflects a generic mechanism present across species for analyzing complex sounds like speech and music; (2) higher-o­ rder sensitivity reflects an adaptation to ecologically relevant sounds such as speech and music in humans or vocalizations in other species; and (3) higher-o­ rder sensitivity reflects a specific adaptation in humans, potentially driven by the unique demands of speech and music perception, that is not generically present in other species even for ecologically relevant sounds. We addressed this question by measuring cortical responses in ferrets – one of the most common animal models used to study auditory cortex (Nelken et al, 2008) – to the same set of natural and synthetic sounds previously tested in humans, as well as natural and synthetic ferret vocalizations

  • The modulation-­matched sounds audibly differ from their natural counterparts, for complex sounds like speech and music that contain higher-o­ rder structure not captured by frequency and modulation statistics

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Summary

Introduction

Little is known about how sensory representations of natural stimuli differ across species (Theunissen and Elie, 2014). Human auditory cortex exhibits preferential responses for speech phonemes (Mesgarani et al, 2014; Di Liberto et al, 2015), but much of this sensitivity can be predicted by simple forms of spectrotemporal modulation tuning (Mesgarani et al, 2014), and perhaps as a consequence can be observed in other animals such as ferrets (Mesgarani et al, 2008; Steinschneider et al, 2013) Consistent with this finding, maps of spectrotemporal modulation, measured using natural sounds, appear coarsely similar between humans and macaques (Erb et al, 2019), temporal modulations present in speech may be over-r­epresented in humans. It remains unclear if the representation of natural sounds in auditory cortex differs substantially between humans and other animals, and if so, how

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