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A physiological signature of sound meaning in dementia.

ABSTRACT: The meaning of sensory objects is often behaviourally and biologically salient and decoding of semantic salience is potentially vulnerable in dementia. However, it remains unclear how sensory semantic processing is linked to physiological mechanisms for coding object salience and how that linkage is affected by neurodegenerative diseases. Here we addressed this issue using the paradigm of complex sounds. We used pupillometry to compare physiological responses to real versus synthetic nonverbal sounds in patients with canonical dementia syndromes (behavioural variant frontotemporal dementia - bvFTD, semantic dementia - SD; progressive nonfluent aphasia - PNFA; typical Alzheimer's disease - AD) relative to healthy older individuals. Nonverbal auditory semantic competence was assessed using a novel within-modality sound classification task and neuroanatomical associations of pupillary responses were assessed using voxel-based morphometry (VBM) of patients' brain MR images. After taking affective stimulus factors into account, patients with SD and AD showed significantly increased pupil responses to real versus synthetic sounds relative to healthy controls. The bvFTD, SD and AD groups had a nonverbal auditory semantic deficit relative to healthy controls and nonverbal auditory semantic performance was inversely correlated with the magnitude of the enhanced pupil response to real versus synthetic sounds across the patient cohort. A region of interest analysis demonstrated neuroanatomical associations of overall pupil reactivity and differential pupil reactivity to sound semantic content in superior colliculus and left anterior temporal cortex respectively. Our findings suggest that autonomic coding of auditory semantic ambiguity in the setting of a damaged semantic system may constitute a novel physiological signature of neurodegenerative diseases.

SUBMITTER: Fletcher PD

PROVIDER: S-EPMC4819950 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Most language users agree that some words sound harsh (e.g. grotesque) whereas others sound soft and pleasing (e.g. lagoon). While this prominent feature of human language has always been creatively deployed in art and poetry, it is still largely unknown whether the sound of a word in itself makes any contribution to the word's meaning as perceived and interpreted by the listener. In a large-scale lexicon analysis, we focused on the affective substrates of words' meaning (i.e. affective meaning) and words' sound (i.e. affective sound); both being measured on a two-dimensional space of valence (ranging from pleasant to unpleasant) and arousal (ranging from calm to excited). We tested the hypothesis that the sound of a word possesses affective iconic characteristics that can implicitly influence listeners when evaluating the affective meaning of that word. The results show that a significant portion of the variance in affective meaning ratings of printed words depends on a number of spectral and temporal acoustic features extracted from these words after converting them to their spoken form (study1). In order to test the affective nature of this effect, we independently assessed the affective sound of these words using two different methods: through direct rating (study2a), and through acoustic models that we implemented based on pseudoword materials (study2b). In line with our hypothesis, the estimated contribution of words' sound to ratings of words' affective meaning was indeed associated with the affective sound of these words; with a stronger effect for arousal than for valence. Further analyses revealed crucial phonetic features potentially causing the effect of sound on meaning: For instance, words with short vowels, voiceless consonants, and hissing sibilants (as in 'piss') feel more arousing and negative. Our findings suggest that the process of meaning making is not solely determined by arbitrary mappings between formal aspects of words and concepts they refer to. Rather, even in silent reading, words' acoustic profiles provide affective perceptual cues that language users may implicitly use to construct words' overall meaning.

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A physiological signature of sound meaning in dementia.

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