Abstract
Abnormal responsiveness to salient sensory signals is often a prominent feature of dementia diseases, particularly the frontotemporal lobar degenerations, but has been little studied. Here we assessed processing of one important class of salient signals, looming sounds, in canonical dementia syndromes. We manipulated tones using intensity cues to create percepts of salient approaching (“looming”) or less salient withdrawing sounds. Pupil dilatation responses and behavioral rating responses to these stimuli were compared in patients fulfilling consensus criteria for dementia syndromes (semantic dementia, n = 10; behavioral variant frontotemporal dementia, n = 16, progressive nonfluent aphasia, n = 12; amnestic Alzheimer's disease, n = 10) and a cohort of 26 healthy age-matched individuals. Approaching sounds were rated as more salient than withdrawing sounds by healthy older individuals but this behavioral response to salience did not differentiate healthy individuals from patients with dementia syndromes. Pupil responses to approaching sounds were greater than responses to withdrawing sounds in healthy older individuals and in patients with semantic dementia: this differential pupil response was reduced in patients with progressive nonfluent aphasia and Alzheimer's disease relative both to the healthy control and semantic dementia groups, and did not correlate with nonverbal auditory semantic function. Autonomic responses to auditory salience are differentially affected by dementias and may constitute a novel biomarker of these diseases.
Highlights
Accurate processing of salient sensory signals is essential in order to negotiate our physical and social environment successfully
Nonverbal sound is well fitted in evolutionary terms to generate salient sensory signals: sounds are our major source of information about the wider sensory environment under conditions of reduced vision, and whether a sound source is approaching or withdrawing is of fundamental behavioral relevance
We have demonstrated that dementia syndromes have dissociable profiles of behavioral and autonomic reactivity to salient sounds
Summary
Accurate processing of salient sensory signals is essential in order to negotiate our physical and social environment successfully. Stimulus salience is carried by a variety of properties ranging from basic perceptual cues such as contrast (brightness, loudness) and motion (approach—withdrawal) to more complex semantic and affective attributes (Fletcher et al, in press); while the processing of salience engages distributed cortico-subcortical neural circuitry (Neuhoff, 2001; Seifritz et al, 2002; Bach et al, 2008; Seeley et al, 2009; Wang et al, 2012; Wang and Munoz, 2014) These circuits include cortical areas in the region of the temporo-parietal junction (in particular, the superior temporal sulcus) representing dynamic changes in auditory and visual stimuli and their. Besides evoking greater behavioral responses, looming sounds are more physiologically arousing, producing greater autonomic responses as indexed by changes in galvanic skin conductance and heart rate, than withdrawing sounds (Bach et al, 2008)
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