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

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. During spoken word processing, the human brain separates lexical meaning from emotional prosody 1-3. Lexical processing entails speech sound sequence recognition and the matching of such sequences to previously associated meanings. This requires access to pre-existing speech sound sequence representations, assumedly involving higher levels of the speech processing hierarchy 3,4. In contrast, emotional prosody processing is largely based upon simple acoustic cues (such as pitch and pitch change) 5-8. In an fMRI study with awake dogs (Canis familiaris) listening to words, we found evidence that the ability to separately process lexical information and emotional prosody is not specific to humans 9. Dogs showed an overall right hemispheric bias for lexically marked (praise) but not for lexically unmarked (neutral) words, independently of emotional prosody. While this initial study identified a set of auditory brain regions in dogs that are responsive to human speech in general, the distribution of labour among these regions remained unclear. To functionally characterize speech-responsive regions and better understand the relationship of lexical and emotional prosody processing in dogs, here we followed up directly on our previous work, using the same stimuli, but applying a multilevel fMRI adaptation paradigm. Habituation/dishabituation paradigms are successfully used in various species, including dogs, to examine whether individuals are able to distinguish among certain stimuli 10,11. This behavioural priming phenomenon is often linked to a reduction in neural activity associated with repeated stimulus processing, which can be measured ...

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