Disturbance of Emotion Processing in Frontotemporal Dementia: A Synthesis of Cognitive and Neuroimaging Findings

Neuroscience Research Australia, Randwick, NSW, Australia.
Neuropsychology Review (Impact Factor: 4.59). 05/2012; 22(3):280-97. DOI: 10.1007/s11065-012-9201-6
Source: PubMed


Accurate processing of emotional information is a critical component of appropriate social interactions and interpersonal relationships. Disturbance of emotion processing is present in frontotemporal dementia (FTD) and is a clinical feature in two of the three subtypes: behavioural-variant FTD and semantic dementia. Emotion processing in progressive nonfluent aphasia, the third FTD subtype, is thought to be mostly preserved, although current evidence is scant. This paper reviews the literature on emotion recognition, reactivity and expression in FTD subtypes, although most studies focus on emotion recognition. The relationship between patterns of emotion processing deficits and patterns of neural atrophy are considered, by integrating evidence from recent neuroimaging studies. The review findings are discussed in the context of three contemporary theories of emotion processing: the limbic system model, the right hemisphere model and a multimodal system of emotion. Results across subtypes of FTD are most consistent with the multimodal system model, and support the presence of somewhat dissociable neural correlates for basic emotions, with strongest evidence for the emotions anger and sadness. Poor emotion processing is evident in all three subtypes, although deficits are more widespread than what would be predicted based on studies in healthy cohorts. Studies that include behavioural and imaging data are limited. Future investigations combining these approaches will help improve the understanding of the neural network underlying emotion processing. Presently, longitudinal investigations of emotion processing in FTD are lacking, and studies investigating emotion processing over time are critical to understand the clinical manifestations of disease progression in FTD.

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    • "Altered processing of sensory signals is an important feature of these diseases (Bathgate et al., 2001; Snowden et al., 2001; Pijnenburg et al., 2004; Jesso et al., 2011; Omar et al., 2011a, 2013; Rohrer et al., 2012; Fletcher et al., 2013; Downey et al., 2014; Landqvist Waldo et al., 2014; Perry et al., 2014; Woolley et al., 2014; Zhou and Seeley, 2014). Patients commonly fail to interpret emotional and social cues correctly (Jesso et al., 2011; Omar et al., 2011a; Kumfor and Piguet, 2012; Zhou and Seeley, 2014) and may show obsessional attachment to particular stimuli such as sweet foods (Woolley et al., 2014) or music (Fletcher et al., 2013) suggesting a generic disturbance in processing reward and attributing hedonic valence (Perry et al., 2014). However, several series have documented symptoms that might signify a more fundamental abnormality in coding somatosensory signals, in particular pain and temperature, by patients with FTLD (Bathgate et al., 2001; Snowden et al., 2001; Ahmed et al., 2015). "
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    ABSTRACT: Symptoms suggesting altered processing of pain and temperature have been described in dementia diseases and may contribute importantly to clinical phenotypes, particularly in the frontotemporal lobar degeneration spectrum, but the basis for these symptoms has not been characterized in detail. Here we analysed pain and temperature symptoms using a semi-structured caregiver questionnaire recording altered behavioural responsiveness to pain or temperature for a cohort of patients with frontotemporal lobar degeneration (n = 58, 25 female, aged 52-84 years, representing the major clinical syndromes and representative pathogenic mutations in the C9orf72 and MAPT genes) and a comparison cohort of patients with amnestic Alzheimer's disease (n = 20, eight female, aged 53-74 years). Neuroanatomical associations were assessed using blinded visual rating and voxel-based morphometry of patients' brain magnetic resonance images. Certain syndromic signatures were identified: pain and temperature symptoms were particularly prevalent in behavioural variant frontotemporal dementia (71% of cases) and semantic dementia (65% of cases) and in association with C9orf72 mutations (6/6 cases), but also developed in Alzheimer's disease (45% of cases) and progressive non-fluent aphasia (25% of cases). While altered temperature responsiveness was more common than altered pain responsiveness across syndromes, blunted responsiveness to pain and temperature was particularly associated with behavioural variant frontotemporal dementia (40% of symptomatic cases) and heightened responsiveness with semantic dementia (73% of symptomatic cases) and Alzheimer's disease (78% of symptomatic cases). In the voxel-based morphometry analysis of the frontotemporal lobar degeneration cohort, pain and temperature symptoms were associated with grey matter loss in a right-lateralized network including insula (P < 0.05 corrected for multiple voxel-wise comparisons within the prespecified anatomical region of interest) and anterior temporal cortex (P < 0.001 uncorrected over whole brain) previously implicated in processing homeostatic signals. Pain and temperature symptoms accompanying C9orf72 mutations were specifically associated with posterior thalamic atrophy (P < 0.05 corrected for multiple voxel-wise comparisons within the prespecified anatomical region of interest). Together the findings suggest candidate cognitive and neuroanatomical bases for these salient but under-appreciated phenotypic features of the dementias, with wider implications for the homeostatic pathophysiology and clinical management of neurodegenerative diseases.
    Brain 10/2015; 138(11). DOI:10.1093/brain/awv276 · 9.20 Impact Factor
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    • "Dementias are generally defined by progressive deterioration in cognitive function but often produce less wellcharacterized alterations in emotional, motivational, and social functions. These alterations are particularly early and significant in behavioral variant frontotemporal dementia (bvFTD) and semantic dementia (SD) within the frontotemporal lobar degeneration (FTLD) spectrum [1] [2] [3] [4] [5] [6] [7] [8], and are probably underrecognized in progressive nonfluentaphasia (PNFA) [9] and Alzheimer's disease (AD) [4,10– 12]. However, although emotional disturbances are hallmarks of many dementias and potentially relevant to disease detection, tracking and therapy, the pathophysiology of disturbed emotion in dementia is poorly understood and challenging to measure objectively. "
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    ABSTRACT: Introduction: Emotional behavioral disturbances are hallmarks of many dementias but their pathophysiology is poorly understood. Here we addressed this issue using the paradigm of emotionally salient sounds. Methods: Pupil responses and affective valence ratings for nonverbal sounds of varying emotional salience were assessed in patients with behavioral variant frontotemporal dementia (bvFTD) (n=14), semantic dementia (SD) (n=10), progressive nonfluent aphasia (PNFA) (n=12), and AD (n=10) versus healthy age-matched individuals (n=26). Results: Referenced to healthy individuals, overall autonomic reactivity to sound was normal in Alzheimer's disease (AD) but reduced in other syndromes. Patients with bvFTD, SD, and AD showed altered coupling between pupillary and affective behavioral responses to emotionally salient sounds. Discussion: Emotional sounds are a useful model system for analyzing how dementias affect the processing of salient environmental signals, with implications for defining pathophysiological mechanisms and novel biomarker development.
    04/2015; 1(2). DOI:10.1016/j.dadm.2015.02.003
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    • "SD is typically characterised as a language disorder, with prominent anomia and loss of general conceptual knowledge. Increasingly , however, it is recognised that deficits in social cognition and emotional functioning are also present in this syndrome (Hsieh et al., 2013a; Irish et al., 2014a; Kumfor et al., 2013, 2011; Kumfor and Piguet 2012; Rankin et al., 2009; Rosen et al., 2002). "
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    ABSTRACT: The ability to perceive, learn and recognise faces is a complex ability, which is key to successful social interactions. This ability is proposed to be coordinated by neural regions in the occipital and temporal lobes, specialised for face perception and memory. While previous studies have suggested that memory for faces is compromised in some dementia syndromes, it remains unclear whether this simply reflects more generalised memory deficits. Here, we examined basic face perception (Identity-Matching), face recognition (Cambridge Face Memory Task) and object recognition (Cambridge Car Memory Task) in 11 semantic dementia (SD) patients (8 left-lateralised, 3 right-lateralised) and 13 behavioural-variant frontotemporal dementia (bvFTD) patients, compared with 11 controls. On the Identity-Matching task, bvFTD were impaired compared to controls, with a similar trend observed in the SD group. Importantly, both bvFTD and SD also demonstrated impaired face recognition. In contrast, only bvFTD showed impaired object recognition, with SD performing within normal limits on this task. Voxel-based morphometry analyses revealed that Identity-Matching and face recognition were associated with partly dissociable regions including the fusiform cortex and anterior temporal lobe. Object-memory was associated with thalamic integrity in the bvFTD group only. These results reveal that face perception and face memory deficits are common in bvFTD and SD, and have been previously underestimated. These deficits are due to neurodegeneration of key regions within the'core' and'extended' face processing system, providing convergent evidence of the neural regions supporting face perception. From a clinical perspective, impaired ability to recognise faces is common in bvFTD and SD and therefore strategies to improve face perception and memory may be beneficial for these patients. Copyright © 2015. Published by Elsevier Ltd.
    Neuropsychologia 03/2015; 71. DOI:10.1016/j.neuropsychologia.2015.03.020 · 3.30 Impact Factor
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