Identification of environmental sounds and melodies in syndromes of anterior temporal lobe degeneration

Abstract

Recognition of nonverbal sounds in semantic dementia and other syndromes of anterior temporal lobe degeneration may determine clinical symptoms and help to define phenotypic profiles. However, nonverbal auditory semantic function has not been widely studied in these syndromes. Here we investigated semantic processing in two key nonverbal auditory domains – environmental sounds and melodies – in patients with semantic dementia (SD group; n = 9) and in patients with anterior temporal lobe atrophy presenting with behavioural decline (TL group; n = 7, including four cases with MAPT mutations) in relation to healthy older controls (n = 20). We assessed auditory semantic performance in each domain using novel, uniform within-modality neuropsychological procedures that determined sound identification based on semantic classification of sound pairs. Both the SD and TL groups showed comparable overall impairments of environmental sound and melody identification; individual patients generally showed superior identification of environmental sounds than melodies, however relative sparing of melody over environmental sound identification also occurred in both groups. Our findings suggest that nonverbal auditory semantic impairment is a common feature of neurodegenerative syndromes with anterior temporal lobe atrophy. However, the profile of auditory domain involvement varies substantially between individuals.

Functional neuroanatomy of speech signal decoding in primary progressive aphasias

“…The lvPPA group showed reduced activation of posterior superior temporal cortex in response to phonemic spectral structure. These syndromic signatures are in accord with prior predictions concerning the informational components of speech signals that are most likely to be vulnerable in each PPA syndrome (Golden et al., 2015, Grube et al., 2016, Hailstone et al., 2012, Hardy et al., 2015, Henry et al., 2016, Hsieh et al., 2011, Lambon Ralph et al., 2010, Rohrer et al., 2010). Performance on post-scan behavioral testing correlated with regional neural activation for the processing of phonemic structure and signal information content for the relevant syndromic (lvPPA and svPPA) groups relative to healthy controls: functional neuroanatomical profiles may therefore underpin behavioral speech processing deficits in these syndromes, though the lack of correlation within the respective patient groups suggests that additional factors may drive individual performance variation.…”

“…Based on the present data in svPPA, we propose that signal entropy accesses a generic neural algorithm that computes and predicts sensory object attributes for further semantic analysis. Interpreted in these terms, the lack of a differential effect of entropy conditions in the nfvPPA and lvPPA groups here would be consistent with a more fundamental impairment of pitch pattern analysis in these syndromes, whereas the differential entropy effect indexed in the svPPA group would reflect a disproportionate deficit in computing object-level statistics in svPPA (Golden et al., 2015, Golden et al., 2016, Hsieh et al., 2011, Lambon Ralph et al., 2010, Rohrer et al., 2012). …”

A physiological signature of sound meaning in dementia

“…We studied patients representing a range of dementia syndromes in order to assess the extent to which putative salience responses might differentiate or transcend syndromic categories. Semantic deficits are not restricted to a particular syndrome: while SD is the paradigmatic disorder of the human semantic system ( Lambon Ralph, Sage, Jones, & Mayberry, 2010 ), less severe or less consistent auditory and other semantic deficits have been documented in each of the other neurodegenerative syndromes included here ( Golden et al., 2015 , Goll et al., 2010a , Goll et al., 2011 , Hardy et al., 2015 , Hsieh et al., 2011 ). Moreover, these diseases have been shown to have distinct profiles of pupil reactivity to salient sounds ( Fletcher et al., 2015c , Fletcher et al., 2015d ).…”

Behavioural and neuroanatomical correlates of auditory speech analysis in primary progressive aphasias

“…In the present study, we set out to identify the critical structural neuroanatomical correlates of psychoacoustic performance on these speech signal characteristics. Drawing on previous neuropsychological evidence, we hypothesised that patients with nfvPPA (but not svPPA) would show impaired processing of temporal regularity [ 8 , 12 , 18 ], while both patient groups would show impaired processing of spectral structure and predictability (fundamental information content) of speech signals [ 5 , 6 , 10 – 12 , 16 , 19 ]. We further hypothesised based on previous neuroanatomical work that the processing of temporal regularity and signal predictability would correlate with grey matter in a distributed frontotemporal–subcortical network comprising the posterior temporal, medial prefrontal and striatal cortex [ 20 – 24 ], while the processing of phonemic spectral structure would correlate with grey matter in the temporo-parietal cortex [ 25 – 28 ].…”