Multilevel fMRI adaptation for spoken word processing in the awake dog brain

Anna Gábor,Enikő Kubinyi,Ádám Miklósi,Dóra Szabó,Attila Andics,Márta Gácsi

doi:10.1038/s41598-020-68821-6

Anna Gábor, Enikő Kubinyi + Show 4 more

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https://doi.org/10.1038/s41598-020-68821-6

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Abstract

Human brains process lexical meaning separately from emotional prosody of speech at higher levels of the processing hierarchy. Recently we demonstrated that dog brains can also dissociate lexical and emotional prosodic information in human spoken words. To better understand the neural dynamics of lexical processing in the dog brain, here we used an event-related design, optimized for fMRI adaptation analyses on multiple time scales. We investigated repetition effects in dogs’ neural (BOLD) responses to lexically marked (praise) words and to lexically unmarked (neutral) words, in praising and neutral prosody. We identified temporally and anatomically distinct adaptation patterns. In a subcortical auditory region, we found both short- and long-term fMRI adaptation for emotional prosody, but not for lexical markedness. In multiple cortical auditory regions, we found long-term fMRI adaptation for lexically marked compared to unmarked words. This lexical adaptation showed right-hemisphere bias and was age-modulated in a near-primary auditory region and was independent of prosody in a secondary auditory region. Word representations in dogs’ auditory cortex thus contain more than just the emotional prosody they are typically associated with. These findings demonstrate multilevel fMRI adaptation effects in the dog brain and are consistent with a hierarchical account of spoken word processing.

Highlights

While long-term fMRI adaptation is thought to have a role in the formation of long-term stored representations and to reflect long-lasting neural sharpening for learned stimuli[19,23]
We found no significant effects of either lexical meaning or emotional prosody with the classic 4-condition-based model, neither in whole-brain tests nor in functionally defined speech-responsive regions (Fig. 1)
The lexical meaning-based short-term fMRI adaptation analyses revealed no significant effects of either repetition or hemisphere, neither in subcortical nor in cortical speech-responsive regions

Summary

Introduction

While long-term fMRI adaptation is thought to have a role in the formation of long-term stored representations and to reflect long-lasting neural sharpening for learned stimuli[19,23]. Auditory fMRI adaptation studies in humans suggest that lexical processing, typically tested by repeated presentations of known words, can be reflected by both long-term[29,30,31] and short-term[32,33] repetition suppression effects. FMRI adaptation appears to provide an efficient means to investigate auditory processing mechanisms in a passive listening paradigm, it has never been exploited in dogs before In this fMRI experiment, dogs listened to lexically and prosodically marked and unmarked words in all combinations. We hypothesized that in dogs, to humans, lexical and prosodic processing are reflected by distinct fMRI adaptation effects in speech-responsive auditory brain regions, and are modulated by age. We predicted that in dogs lexical meaning-based adaptation (1) would be independent of prosody effects at higher levels of the processing hierarchy, and (2) would exhibit right hemisphere dominance

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