Emotion recognition in Huntington's disease and frontotemporal dementia

Neuropsychologia 46 (2008) 2638–2649

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Emotion recognition in Huntington’s disease and frontotemporal dementia J.S. Snowden a,∗ , N.A. Austin b , S. Sembi c , J.C. Thompson a , D. Craufurd d , D. Neary a a Cerebral Function Unit, Greater Manchester Neuroscience Centre, Salford Royal Foundation Trust and Clinical Neurosciences Research Group, University of Manchester, United Kingdom b Department of Psychology, The Adelaide and Meath Hospital, Dublin, Ireland c Bristol Doctorate in Clinical Psychology, University of Plymouth, United Kingdom d Medical Genetics Research Group, University of Manchester, United Kingdom

a r t i c l e

i n f o

Article history: Received 18 November 2007 Received in revised form 18 April 2008 Accepted 27 April 2008 Available online 2 May 2008 Keywords: Affect Disgust Anger Degenerative disease

a b s t r a c t A well-documented feature of Huntington’s disease (HD) is disproportionate impairment in the ability to recognise the emotional expression of disgust. However, this finding has been challenged by studies that report no differential disgust impairment and attribute apparent differences across emotions to task difficulty. The present study sought to shed light on disparities in findings through a comparative study of emotion recognition in HD and frontotemporal dementia (FTD). Ten HD, 12 FTD patients and 12 healthy controls were administered 10 tasks assessing facial and vocal recognition of emotions and comprehension of emotion terms. The findings were not consistent with either the ‘selective disgust impairment’ or ‘task difficulty’ view. Both HD and FTD groups were impaired compared to controls, deficits in HD being less severe. Impairments in FTD were elicited for all emotions whereas in HD they were demonstrated predominantly for negative emotions of fear, disgust and anger. Consistency in performance, despite varying task demands, excluded an explanation in terms of item difficulty, and was in keeping with the notion of distinct neural substrates for processing of negative emotions. Contrary to the notion of disproportionate disgust impairment, the most severe deficits in HD were elicited for anger, a finding that may have relevance for the poor anger control that is the hallmark of HD. The data raise the possibility that linguistic influences and conceptual complexities of the emotion of disgust may contribute to the variable finding of selective disgust impairment in HD. © 2008 Elsevier Ltd. All rights reserved.

1. Introduction Recent years have seen a burgeoning of interest in the way that brain lesions alter the recognition and expression of emotion. The interest has been stimulated in large part by reports that the recognition of specific emotions may be compromised selectively. An association is well documented between impaired recognition of facial expressions of fear and lesions of the amygdala (Adolphs, Tranel, Damasio, & Damasio, 1994, 1995; Broks et al., 1998; Calder et al., 1996; Sato et al., 2002; Scott et al., 1997). More recently, selective impairment of anger recognition has been reported in association with lesions of the ventral striatum (Calder, Keane, Lawrence, & Manes, 2004) and disgust with lesions of the insula (Calder, Lawrence, & Young, 2001).

∗ Corresponding author at: Cerebral Function Unit, Greater Manchester Neuroscience Centre, Hope Hospital, Salford M6 8HD, United Kingdom. Tel.: +44 161 206 2561. E-mail address: [email protected] (J.S. Snowden). 0028-3932/$ – see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.neuropsychologia.2008.04.018

A prominent source of evidence for the selective (or disproportionate) impairment of disgust recognition comes from patients with Huntington’s disease (HD), an inherited neurodegenerative disorder characterised by involuntary movements, cognitive impairment and behavioural changes. Disgust impairment has been demonstrated not only in clinically affected patients (Sprengelmeyer et al., 1996; Sprengelmeyer et al., 1997; Wang, Hoosain, Yang, Meng, & Wang, 2003), but also in people in the preclinical phase, before symptoms of disease become manifest (Gray, Young, Barker, Curtis, & Gibson, 1997; Hennenlotter et al., 2004; Sprengelmeyer, Schoeder, Young, & Epplen, 2006). These findings are theoretically important because, together with the data relating to fear, they provide the crucial double dissociation in emotion recognition. They indicate that selective impairments should not be dismissed as artefacts of differential difficulty of individual emotions. Rather they point to distinct neural substrates underlying different emotions. Disgust impairment in HD has potential clinical relevance too. It might contribute to understanding of the increased neglect of self-care and personal hygiene that is sometimes associated with HD (Craufurd, Thompson, & Snowden, 2001).

J.S. Snowden et al. / Neuropsychologia 46 (2008) 2638–2649

Nonetheless, the finding of selective/disproportionate disgust impairment in HD is intriguing. HD is predominantly, although not exclusively, a disorder of the striatum. Caudate nucleus and putamen are early sites of pathological change (Aylward et al., 2000; Campodonico et al., 1998; Douaud et al., 2006) and sites of maximal pathological change at end stage disease (De La Monte, VonSattel, & Richardson, 1988; Mann, Oliver, & Snowden, 1993). The demonstrated link between anger recognition and the striatum (Calder et al., 2004) might suggest that anger and not disgust ought to be disproportionately affected. Such a prediction is reinforced by HD patients’ clinical characteristics. A prominent behavioural feature in HD is increased irritability, aggressive outbursts and poor temper control (Craufurd et al., 2001; Thompson, Snowden, Craufurd, & Neary, 2002). If the expression of anger is influenced by the disease process, then it might be anticipated that its recognition would also be compromised. Selective disgust recognition impairment in HD is, moreover, not a universal finding. Milders, Crawford, Lamb, and Simpson (2003) and Johnson et al. (2007) reported no evidence of selectivity. These authors acknowledged that negative emotions (fear, anger, disgust) were more severely affected than positive emotions (happiness, surprise). However, Milders et al. ascribed this to the greater difficulty of recognition of negative emotions, and explicitly rejected the notion of differential impairment. Thus, the status of emotion recognition in HD remains controversial, and the basis of the disparity in findings across studies is uncertain. The present study sought to shed light on the conflicting findings. Two strategies were adopted to help to clarify the status of emotion recognition in HD: (a) inclusion of a separate pathological group for comparison and (b) inclusion of a range of emotion tasks that make distinct demands. Studies of emotion recognition have hitherto been confined to a single diagnostic group. Compelling evidence of dissociated breakdown in emotion recognition would come from a demonstration of distinct pathological performance profiles within the same study, comparing profiles on identical measures. A neurodegenerative disorder for which emotional changes are a central feature is frontotemporal dementia (FTD). In contrast to HD in which pathological change is most marked in the striatum, FTD is predominantly a neocortical disorder, involving degeneration of the frontal and anterior temporal lobes (Mann & South, 1993; Snowden, Neary, & Mann, 1996). It is associated with radical alterations in the patients’ character and breakdown in social conduct, and impairments in executive functions (Neary, Snowden, & Mann, 2005; Snowden et al., 1996). Presenting symptoms are commonly of an affective nature. For example, relatives may comment on the patient’s failure to show normal emotions of grief at a family funeral or to show sympathy at a friend’s misfortune. Patients commonly display a blunting of affect. Their failure to exhibit both basic (happiness, sadness, anger, fear, surprise, disgust) and social emotions (embarrassment, empathy, sympathy) strongly differentiates FTD from Alzheimer’s disease and vascular dementia and is an important predictor of the disorder (Bathgate, Snowden, Varma, Blackshaw, & Neary, 2001). Complementing these findings studies have demonstrated widespread impairment in FTD patients in the recognition of both facial (Keane, Calder, Hodges, & Young, 2002; Lavenu & Pasquier, 2005; Lavenu, Pasquier, Lebert, Petit, & Van der Linden, 1999; Lough et al., 2006) and vocal (Keane et al., 2002) expressions of emotion. If disproportionate impairment in disgust recognition is truly a core feature of HD then one would predict distinct performance profiles in HD and FTD. In both groups impaired recognition of emotions would be anticipated, but only HD patients should show a disproportionate impairment in disgust recognition. Impairments in recognition of facial emotions, reported in the published literature, have typically been demonstrated using the

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Ekman series of faces (Ekman & Friesen, 1976). This uniformity in test methodology has the distinct advantage of allowing direct comparisons across studies. However, a disadvantage is that genuine effects of emotion (predicted by Sprengelmeyer et al.) cannot always easily be disentangled from the effects of item difficulty (predicted by Milders et al.). The use of diverse tasks, including distinct sets of faces, offers the potential to distinguish these factors because ‘difficulty’ would be predicted to vary according to task. The eye region of the face, for example, is regarded as particularly crucial for the recognition of fear, sadness and anger (Adolphs et al., 2005), whereas the mouth is highly informative in the case of happiness. Happiness might therefore be expected to be an easy emotion to recognise from full face but relatively difficult from eyes alone. Disgust might be expected to be relatively difficult from facial expression because of visual similarities with anger, but relatively easy from vocal expression because of its auditory distinctiveness. If the nature of the emotion per se is a critical factor in influencing HD performance then a similar performance profile ought to be elicited across diverse tasks. By contrast, if performance is a product of item difficulty then distinct patterns of impairment ought to be demonstrated. Although the strategies of comparing pathological groups and including diverse tasks may help to adjudicate between ‘selective disgust’ and ‘task difficulty’ accounts of emotion recognition in HD they do not directly address the possible causes of disparities in findings in the literature. A number of factors might potentially contribute to those disparities. These include stage of illness, clinical heterogeneity and linguistic/cultural factors. A selective disgust disorder might, for example, be present early in the course of disease, and give way to a more generalised impairment of emotions later in the course. This would be a reasonable proposition in view of the fact that selective disgust impairments have been elicited as commonly in the pre-clinical phase (Gray et al., 1997; Hennenlotter et al., 2004; Sprengelmeyer et al., 2006) as in clinically established HD. Direct comparison of overall level of performance of participants, elicited in different studies using the same test methodology, would allow the potential influence of overall severity to be addressed. Clinical heterogeneity is an important consideration. People with HD are known to differ in terms of the precise characteristics of their motor and cognitive disorder and these differences have been found to be associated with different topographical distributions of atrophy (Rosas et al., 2008). It would be reasonable to expect that differences might be present too in the precise nature of changes in emotion processing. Examination of individual as well as group performance profiles would help to address the question of phenotypic variation in HD. The most compelling demonstrations of selective disgust impairment in HD come from studies of German-speaking patients (Sprengelmeyer et al., 1996, 1997, 2006), raising the question of whether linguistic or cultural factors might influence results. Emotion tasks almost invariably have a verbal component. They involve matching an emotive stimulus, usually a facial or vocal expression, with a verbal label. Although deficits are typically ascribed to recognition of the emotive stimulus itself, precision of understanding of the verbal label might also potentially influence performance. Although a multicultural investigation is beyond the scope of the present study, inclusion of tests that (a) explicitly address understanding of emotion terms and (b) make no verbal demands might help to determine whether linguistic factors play in role. It might be anticipated that linguistic factors would influence performance in HD less than in FTD. FTD is associated with cortical pathology, which may impinge on language areas. Moreover, behavioural characteristics of FTD patients, such as economy of mental effort and little concern for performance accuracy, suggest

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that their performance on emotion tasks is likely to be influenced by the task’s executive demands. The inclusion of simplified test procedures that minimise executive demands, eliminate the need for comprehension of verbal labels and control for perceptual abnormalities permits the possibility of distinguishing genuine impairments in emotion recognition from other cognitive factors that might influence test performance. A closer relationship between performance on emotion recognition and standard executive tasks might be predicted in FTD than in HD. The present study aims to clarify the nature of emotion recognition in HD and to help to resolve apparent disparities in findings in the literature. The study addresses the prediction that there are distinct profiles of impairment in emotion recognition in HD and FTD, and that a disproportionate impairment in the recognition of disgust is present in HD. It examines too the hypothesis that differences in performance across emotions is a product of differences in task difficulty. It explores potential influences on performance such as severity of illness, clinical heterogeneity, language and executive functions. 2. Participants The participants comprised 10 patients with HD, 12 with FTD and 12 healthy controls. The HD patients (five men and five women) had clinically established and genetically confirmed HD and all attended a regional specialist HD clinic. Their mean age at the time of testing was 47 (S.D. 9) years, and they had been symptomatic for an average of 7 (S.D. 3) years. The FTD group consisted of 12 patients (10 men and 2 women) who fulfilled clinical criteria for FTD (Neary et al., 1998). All patients were attending a specialist early onset dementia clinic, and had presented to medical attention with a progressive history of personality change and breakdown in interpersonal conduct, with social disinhibition, neglect of self-care and neglect of personal and domestic responsibilities. Patients were excluded from the study if there was evidence from history or neurological examination of vascular disease, head trauma or other coincidental pathology that might influence the patient’s mental state. The FTD patients’ mean age at the time of testing was 65 (S.D. 8) years. This is significantly older than the HD group (U = 7.5, p < 0.01), and reflects the later onset age of FTD compared to HD. They had a mean illness duration of 5 (3) years (S.D. 3.2), which does not differ significantly from that of the HD patients. The control group consisted of 12 healthy volunteers, 8 men and 4 women, who responded to an advertisement. They had no history of neurological disease, head injury or alcohol abuse. Their mean age was 57 (S.D. 9) years, which was not significantly different from means for either FTD or HD groups. Informed written consent was obtained from all participants and/or their next of kin. The study was granted approval by the local Ethics committee. 3. Methods 3.1. Background neuropsychological assessment All participants were administered background neuropsychological tests of language, visual perception, spatial skills, memory and executive abilities: graded naming test (McKenna & Warrington, 1983), subtests of the visual object and space perception battery (Warrington & James, 1991), Benton face recognition test (Benton, Hemsher, Varney, & Spreen, 1983), Hopkins verbal learning test (Brandt, 1991), a locally developed recall and forced-choice recognition picture memory test (Stopford, Snowden, Thompson, & Neary, 2007), the modified Wisconsin card sorting test (Nelson, 1976), Weigl’s block test (De Renzi, Faglioni, Savoiardo, & Vignolo, 1966), letter and category fluency (Spreen & Strauss, 1991) and a widely used version of the Stroop test (Golden, 1978).

3.2. Emotion assessment Ten tests were included in the emotion battery. Tasks 1–3 assessed verbal comprehension of emotion terms. Tasks 4–6 examined recognition of facial expressions of emotion using materials derived from the Ekman series of faces. Task 7 served as a control task and assessed recognition of facial identity. Task 8 assessed understanding of vocal expressions of emotion. Task 9 assessed recognition of facial expressions of emotion using a novel series of faces and task 10 recognition of emotion from the eyes only. 3.2.1. Task 1: definition of emotion labels Participants were presented with a printed sheet containing the six primary emotion words happiness, surprise, fear, sadness, disgust and anger and asked to explain the meaning of each term. Responses were recorded verbatim. Definitions were later rated by an independent judge, blind to patient identity and experimental group, on a scale of 0–3 (0 = incorrect response; 1 = vague response or concrete example, e.g. happiness—“when I’m with my family”; 2 = acceptable definition that does not fully capture the emotion’s meaning; 3 = good definition). A second independent blind rater was used to determine inter-rater reliability. 3.2.2. Task 2: multiple-choice comprehension of emotion terms and situations Participants were asked a series of 36 questions and instructed to respond by pointing to the appropriate emotion term (happiness, surprise, fear, sadness, disgust and anger) on the response sheet. Twelve questions constituted requests for identification of synonyms (e.g. “Which word means something like scared?”), whereas 24 asked how the person would feel in a particular situation (e.g. “How would you feel if you heard some bad news?”). Six items pertained to each emotion (two synonyms and four situations). The test items were drawn from a larger set of 48 items administered in a pilot study to a control sample of 16 volunteers. Items achieving the greatest response agreement were selected for use as test stimuli. 3.2.3. Task 3: binary-choice comprehension of emotional situations This task was similar to the multiple-choice task, except that the participant was required to select a response from two rather than six emotion terms. The task consisted of 30 items, 5 pertaining to each emotion. Each permutation of emotion-pairs was used twice as response alternatives. The test items were drawn from a larger set of 42 items, and selected on the basis of consistency of response in volunteers in a pilot study. 3.2.4. Task 4: facial expression of emotion: multiple-choice face-label matching (Ekman faces) The test used materials derived from the Ekman and Friesen (1976) series and published in the facial expressions of emotion: stimuli and tests (FEEST) battery (Young, Perrett, Calder, Sprengelmeyer, & Ekman, 2002). The test consisted of 60 faces which the participant was required to match with one of the following verbal labels: happiness, surprise, fear, sadness, disgust and anger. 3.2.5. Task 5: facial expression of emotion: two-choice face-label matching This task was a less demanding version of the above test, designed to reduce the executive demands that might influence patient performance. The stimuli consisted of 60 faces drawn from the FEEST (Young et al., 2002). They were displayed one to a page, below which were two emotion words (e.g. ANGER and DISGUST). Participants were required to select the word best describing the facial expression. The position of the correct response (on the left or the right) was counterbalanced. 3.2.6. Task 6: facial expression of emotion: two-choice face–face expression matching This task was designed to eliminate the possible confounding effect of poor comprehension of emotion labels on performance. Forty-eight plates were produced, each showing three faces (Fig. 1(a)). The upper image (“target”) showed a female actor expressing an emotion. The lower images were of the same male actor, in one case showing the same emotion as the target and in the other case a different emotion. Participants were asked to select the face expressing the same emotion (expression match) as the target. Only faces displaying the negative emotions of fear, sadness, disgust and anger were used. There were 12 examples of each of these 4 emotions, the correct alternative being paired with the other 3 emotions an equal number of times. 3.2.7. Task 7: facial identity: two-choice face–face identity matching This task was included as a perceptual control to task 6, designed to rule out general perceptual impairment as a possible explanation for poor emotion recognition performance. The test materials comprised 48 plates, each showing three faces (Fig. 1(b)). The upper face displayed a neutral expression and the lower two faces the same non-neutral expression (either fear, sadness, disgust or anger). The participant was asked to select the lower image that showed the same person (identity match) as the upper target image.

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Fig. 1. Examples of test items used in (a) task 6, involving matching faces sharing a common emotion and (b) task 7, involving matching faces with the same identity.

3.2.8. Task 8: vocal expression of emotion: multiple-choice sound-label matching A set of recorded stimuli were used (Calder, Keane, Manes, Antoun, & Young, 2000; Keane et al., 2002; Scott et al., 1997) comprising 120 emotional sounds, 20 sounds for each of the 6 emotion categories. Sounds included laughter (happiness), gasps (surprise), screams (fear), sobbing (sadness), retches (disgust), and growls (anger). Sounds were played in turn to participants who were required to select from six printed emotion terms, the one best describing the sound. 3.2.9. Task 9: facial expression of emotion, Manchester face set: recognition of expression from full face This locally developed test (Whittaker, Connell, & Deakin, 1994; Whittaker, Deakin, & Tomenson, 2001) parallels the Ekman faces test, with the exception that it includes ‘neutral’ faces. The participant was required to match a series of 35 photographs of faces conveying facial expressions with the corresponding affect label. The faces were all full-face frontal views (Fig. 2(a)) of actors whose had posed for photograph immediately after hearing a descriptive vignette explicitly designed to facilitate a naturalistic expression of the required emotion. The 35 test photographs were drawn from a larger set of photographs and were selected on the basis that they elicited a consistent affect labelling response in keeping with the intended emotion (cut-off criterion = 80% agreement), in 10 healthy subjects who took part in a reliability study. The test was preceded by five practice items. 3.2.10. Task 10: recognition of emotional expression from eyes only In this locally developed test the participant was shown only the eye and eyebrow region of faces used in task 9 (Fig. 2(b)). The test was preceded by five practice items. 3.3. Statistical analysis Initial explorations of the data showed variable skewing, which could not be uniformly rectified by application of transformations. There were some ceiling level scores in controls, calling into question the interval nature of data points. Heterogeneity in population variances were outside the bounds of acceptability for analysis of variance. For these reasons, non-parametric analyses were used throughout. Kruskal–Wallis analyses of variance were conducted for overall group comparisons, followed by planned Mann–Whitney tests. For within group comparisons Friedman and Wilcoxon tests were used. Two-tailed tests were adopted to avoid prior assumptions regarding the relationship between performance in FTD and HD. Significance levels were set conventionally at p = 0.05, in line with other studies (Calder et al.,

2004; Keane et al., 2002; Milders et al., 2003; Sprengelmeyer et al., 2006). We, like others, were keen to avoid loss of power that would be associated with stringent correction procedures in relatively small samples, and in some tasks with relatively small number of test items. However, most significance levels were sufficiently high to survive correction. Moreover, those findings with significance levels at p < 0.05 were internally consistent with other findings suggesting that they are unlikely to have arisen spuriously.

4. Results 4.1. Background neuropsychological tests The patient groups exhibited a characteristic and expected profile of cognitive performance (Table 1). HD patients showed greatest impairment relative to controls for time-based executive tasks, namely, fluency and Stroop tests. Consistent with previous reports (Snowden, Craufurd, Griffiths, Thompson, & Neary, 2000) impairments were present for low-demand components of the Stroop test as well as the more demanding Interference condition. On memory testing the HD group differed from controls only in giving more false positive, intrusion errors on the yes/no recognition component of the Hopkins test. HD patients performed more poorly than controls on the demanding Benton face recognition test. In the FTD group performance was, as expected, particularly impaired on standard executive tests. Deficits were present on both timed (animal and letter fluency, Stroop) and untimed (modified Wisconsin card sort, Weigl’s blocks) tests. The patients also performed more poorly on tests of memory, showing a characteristic ‘frontal’ pattern of deficits. They were less efficient than controls in carrying out a list learning task, but there was no abnormal loss of information over a delay. On a yes/no recognition memory test for words they made more false positive (intrusion) errors than controls, yet on a four-choice alternative picture recognition

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Fig. 2. Examples of test items from the Manchester face set used in (a) task 9 and (b) task 10.

Table 1 Background neuropsychological assessment Test

FTD

HD

Control

MMSE/30 National adult Reading test errors Graded naming task/30 VOSP dots/10 VOSP position discrimination/20 VOSP cube analysis/10 Benton face recognition test Hopkins verbal learning trials 1–3/36 Hopkins delayed recall/12 Hopkins loss over delay (trial 3-delayed) Hopkins delayed recognition (true positives) Hopkins delayed recognition (false positives) Visual object memory recall/20 Visual object memory recognition/20 WCST categories/6 WCST total errors (max 48) Weigl’s test/9 Letter fluency (total FAS/3 min) Category fluency animals/1 min Stroop word reading/number in 45 s Stroop colour naming/number in 45 s Stroop interference/number in 45 s Stroop interference errors

25 (3)*** 27 (10)**

27 (2)** 22 (9)

29 (1) 18 (6)

16 (8) 9 (2) 19 (2)

19 (5) 9 (2) 18 (3)*

22 (4) 10 (1) 20 (1)

7 (3) 41 (7)** 16 (8)**

8 (3) 41 (4)** 21 (5)

9 (1) 49 (5) 25 (4)

5 (3)* 1 (2)

7 (2) 1 (1)

8 (3) 2 (4)

10 (3)

10 (2)

11 (1)

4 (4)*

3 (3)*

1 (1)

4 (3)** 15 (3)

8 (4) 16 (1)

9 (3) 17 (1)

3 (2)* 26 (15)* 5 (3)*** 22 (20)** 12 (6)*** 70 (27)**

4 (2) 16 (10) 8 (2) 26 (18)** 13 (6)** 50 (14)***

4 (2) 13 (12) 9 (0) 48 (14) 23 (5) 96 (5)

49 (24)*

41 (12***

71 (8)

24 (18)*

23 (5)***

39 (7)

4 (5)**

1 (1)

0 (0)

Asterisks show significant difference from control performance: *p < 0.05; **p < 0.01; ***p < 0.001.

memory test performance did not differ significantly from that of controls. Like the HD patients, FTD patients showed poorer performance on the demanding Benton face recognition test. However, they performed normally on tests of spatial abilities. Comparisons between HD and FTD patients revealed a single group difference only: FTD patients performed more poorly than HD patients on the free recall component of the Manchester visual object memory test. Other comparisons were not significant. The general absence of differences indicates that the FTD and HD groups are broadly matched in terms of their overall level of cognitive impairment. 4.2. Assessment of emotion Mean scores for each group on each of the 10 emotion tasks is shown in Table 2. 4.2.1. Task 1: definition of emotion labels The groups did not differ in their ability to define the terms happiness, surprise, fear, sadness, and anger. However, there was a significant group difference for the term ‘disgust’ (Kruskal–Wallis H = 8.8, p = 0.01). This reflected less precise definitions in the FTD group compared to both HD (U = 29.0, z = −2.3, p = 0.02) and controls (U = 28.5, z = −2.8, p = 0.006). The Kappa statistic revealed an inter-rater reliability in classification of emotion definitions on a four-point scale of 0.79. This overall measure masked substantial differences in agreement between rater for different emotions. Precise agreement was highest for sadness (0.95) and lowest for disgust (0.53). Exploration of the basis for the low agreement for disgust revealed that whereas definitions for other emotions tapped a relatively uniform and constrained dimension of emotion, those for disgust were more variable. Some definitions (21%) related to the visceral feeling of revulsion/nausea arising from an unpleasant visual, olfactory, gustatory or tactile experience, whereas others centred on moral feelings

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Table 2 Performance (mean and S.D.) on emotion tasks in HD, FTD and control group Happiness

Surprise

Fear

Sadness

Disgust

Anger

Task 1 HD FTD Control

2.1 (0.7) 1.8 (0.9) 2.3 (0.8)

2.2 (1.0) 2.0 (1.2) 2.5 (0.8)

1.9 (1.1) 1.7 (1.2) 2.6 (0.8)

2.0 (1.1) 1.6 (1.2) 2.1 (1.0)

1.2 (1.1) 0.3 (0.9) 1.8 (1.3)

2.0 (1.2) 1.3 (1.2) 2.1 (0.9)

Task 2 HD FTD Control

5.7 (0.7) 4.9 (1.2) 5.8 (0.4)

4.4 (1.8) 3.7 (2.1) 5.7 (0.7)

5.3 (0.7) 3.8 (1.6) 5.8 (0.5)

5.3 (1.3) 3.4 (2.2) 5.9 (0.3)

4.6 (1.2) 3.3 (2.0) 5.8 (0.5)

5.3 (0.8) 3.5 (2.2) 5.8 (0.4)

Task 3 HD FTD Control

5.0 (0.0) 4.8 (0.6) 5.0 (0.0)

5.0 (0.0) 4.7 (0.6) 5.0 (0.0)

4.9 (0.3) 4.5 (0.8) 5.0 (0.0)

4.9 (0.3) 4.0 (1.0) 5.0 (0.0)

4.8 (0.4) 4.3 (0.4) 5.0 (0.0)

5.0 (0.0) 4.0 (1.5) 5.0 (0.0)

Task 4 HD FTD Control

9.9 (0.3) 8.3 (2.1) 9.9 (0.3)

6.9 (2.0) 5.8 (2.9) 8.6 (1.4)

3.8 (2.6) 3.0 (2.2) 6.5 (2.4)

6.0 (2.7) 4.4 (3.0) 8.3 (1.3)

5.1 (2.4) 5.8 (2.0) 7.8 (2.1)

3.8 (1.5) 4.6 (3.4) 7.5 (1.6)

Task 5 HD FTD Control

9.9 (0.3) 9.7 (0.7) 10.0 (0.0)

8.8 (1.3) 7.9 (1.6) 9.6 (0.7)

8.4 (1.8) 7.3 (2.6) 9.8 (0.5)

8.6 (1.6) 6.7 (2.8) 9.4 (0.8)

9.5 (1.3) 8.4 (1.3) 9.4 (0.7)

7.9 (1.5) 7.9 (1.7) 9.9 (0.3)

Task 6 HD FTD Control

– – –

– – –

9.8 (1.8) 9.5 (2.4) 11.4 (0.8)

10.2 (2.1) 8.9 (2.4) 11.6 (0.8)

7.2 (2.9) 6.2 (2.7) 10.8 (0.9)

8.3 (1.5) 8.8 (1.6) 10.6 (1.1)

Task 7 HD FTD Control

– – –

– – –

10.2 (1.1) 10.2 (2.3) 11.4 (0.9)

11.3 (1.6) 10.0 (2.1) 11.6 (0.7)

10.7 (1.3) 9.7 (2.6) 11.3 (0.8)

11.2 (1.0) 10.1 (1.7) 11.7 (0.7)

Task 8 HD FTD Control

13.5 (2.8) 11.8 (4.7) 14.8 (2.6)

16.2 (3.3) 12.4 (6.7) 17.9 (1.7)

11.2 (4.0) 9.3 (6.2) 17.0 (2.4)

13.8 (4.4) 12.8 (6.3) 17.3 (1.4)

15.4 (5.5) 13.2 (7.1) 19.6 (1.0)

6.8 (3.9) 6.0 (4.7) 12.6 (3.1)

Task 9 HD FTD Control

4.0 (0.9) 3.8 (1.3) 4.6 (0.7)

2.3 (1.5) 1.2 (1.0) 2.4 (1.2)

2.0 (1.5) 1.6 (1.4) 3.2 (1.7)

3.3 (1.5) 3.2 (1.6) 4.3 (0.9)

2.9 (1.6) 1.5 (1.4) 4.3 (1.2)

1.4 (1.4) 1.7 (1.4) 3.3 (1.1)

Task 10 HD FTD Control

2.1 (1.1) 1.7 (1.8) 2.8 (1.2)

1.2 (1.2) 1.8 (1.4) 1.8 (1.1)

1.9 (1.4) 0.9 (1.3) 2.7 (1.6)

2.2 (1.5) 2.1 (1.3) 3.4 (0.5)

1.1 (0.7) 1.3 (1.2) 2.6 (1.0)

0.9 (0.7) 1.2 (1.2) 1.7 (1.2)

Task 1: defining emotion labels (max = 3); task 2: multiple-choice comprehension of emotion terms and situations (max = 6); task 3: two-choice comprehension of emotional situations (max = 5); task 4: facial emotions—multiple-choice face-label match (Ekman faces) (max = 10); task 5: facial emotions—two-choice face-label match (Ekman faces) (max = 10); task 6: facial emotions—two-choice face–face expression match (max = 12); task 7: control task—two-choice face–face identity match (max = 12); task 8: vocal emotions—multiple-choice sound-label match (max = 20); task 9: Manchester faces—emotion recognition from full face (max = 5); task 10: Manchester faces—emotion recognition from eyes only (max = 5).

of outrage (47%) or general dislike (15%) of behaviour, actions and events. Remaining definitions provided none of these connotations. The visceral-moral spectrum was represented by all three groups, and chi-squared analysis revealed no group differences in frequencies of revulsion vs. moral outrage-type definitions. 4.2.2. Task 2: multiple-choice comprehension of emotion terms and situations The groups differed significantly in their ability to match emotional situations with the appropriate emotion. Most marked differences were present for negative emotions: fear (H = 10.9, p = 0.004), sadness (H = 12.8, p = 0.002), disgust (H = 15.6, p < 0.001), and anger (H = 11.2, p = 0.004). Milder differences were elicited for positive emotions of happiness (H = 6.6, p = 0.04) and surprise (H = 7.7, p = 0.02). Paired group comparisons showed that HD patients performed more poorly than controls only for the emotion of disgust (U = 21.0, z = −2.8, p = 0.005).

FTD patients performed more poorly than controls for all emotions (happiness U = 38, z = −2.3, p = 0.02; surprise U = 28.5, z = −2.7, p = 0.007; fear U = 24.0, z = −3.0, p = 0.003; sadness U = 20.5, z = −3.33, p = 0.001; disgust U = 12.0, z = −3.6, p < 0.001; anger U = 23.0, z = −3.1, p = 0.002). They also performed more poorly than HD patients for fear (U = 28.5, z = −2.1, p = 0.03), sadness (U = 29.0, z = −2.1, p = 0.04), and anger (U = 30.5, z = −2.0, p = 0.05). 4.2.3. Task 3: binary-choice comprehension of emotional situations There was an overall effect of group for the emotions of sadness (H = 12.8, p = 0.002), disgust (H = 6.6, p = 0.04) and anger (H = 10.4, p = 0.006). This reflected poorer performance in FTD patients compared to controls for sadness (U = 30.0, z = −3.0, p = 0.002) disgust (U = 42.0, z = −2.4, p = 0.02) and anger (U = 42.0, z = −2.4, p = 0.02) and compared to HD patients for sadness (U = 29.0, z = −2.4, p = 0.02) and anger (U = 35.0, z = −2.3, p = 0.02) only. The HD group did not differ significantly from controls.

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Fig. 3. Mean scores and standard error in HD, FTD and control groups for six emotions for (a) task 1 (Ekman faces-emotion label match), (b) task 8 (sound-emotion label match), task 9 (Manchester faces-emotion label match, and (d) task 10 (eyes-only-emotion label match).

4.2.4. Task 4: facial emotion: multiple-choice face-label matching (Ekman faces) Group comparisons (Fig. 3(a)) revealed a significant overall group difference for all emotions: happiness (H = 13.3, p = 0.001), surprise (H = 7.6, p = 0.02), fear (H = 10.5, p = 0.005), sadness (H = 10.7, p = 0.005), disgust (H = 8.3, p = 0.02), and anger (H = 11.4, p = 0.003). Paired group comparisons showed that HD patients performed more poorly than controls for all emotions except for happiness (surprise U = 29.5, z = −2.1, p = 0.04; fear U = 25.5, z = −2.3, p = 0.02; sadness U = 30.5, z = −2.0, p = 0.05; disgust U = 23.0, z = −2.5, p = 0.01; anger U = 6.0, z = −3.6, p < 0.001). FTD patients performed more poorly than controls for all emotions (happiness U = 27.5, z = −3.0, p = 0.003; surprise U = 28.5, z = −2.5, p = 0.01; fear U = 19.5, z = −3.1, p = 0.002; sadness U = 19.0, z = −3.1, p = 0.002; disgust U = 31.0, z = −2.4, p = 0.02; anger U = 36.0, z = −2.1, p = 0.04). They performed more poorly than HD patients only for happiness (U = 23.5, z = −2.7, p = 0.007). Within group comparisons of control performance showed that emotions were not equated for difficulty (Friedman 2r = 24.9, p < 0.001). Happiness was recognised by controls significantly better than all other emotions (range anger p = 0.002–surprise p = 0.02). Examination of errors indicated a similar pattern across the three groups. In particular surprise was most often misinterpreted as fear and fear as surprise, whereas anger and disgust were most often confused with each other. False positive errors were distributed across the emotion labels and there was no evidence of a disproportionate bias in one group towards one emotion label that might lead to spurious accuracy scores for that emotion. Examination of scores of individual patients revealed a relatively uniform pattern across individuals, consistent with the overall group findings. No patient in the HD group achieved lowest scores for the emotion of disgust.

4.2.5. Task 5: facial expression of emotion: two-choice face-label matching On this binary choice test there were small overall differences in performance between HD patients and controls (U = 30.0, −z = −2.0, p = 0.05) and larger differences between FTD patients and controls (U = 17.0, z = −3.2, p = 0.001). Differences between HD and FTD did not reach significance. HD patients performed more poorly than controls for fear (U = 33.0, z = −2.0, p = 0.04) and anger (U = 13.5, z = −3.5, p = 0.001) only. In FTD significant impairments were present for all emotions except happiness: surprise U = 24.5, z = −2.9, p = 0.004; fear U = 25.5, z = −2.9, p = 0.004; sadness U = 32.5, z = −2.4, p = 0.02; disgust U = 34.5, z = −2.3, p = 0.02; anger U = 20.5, z = −3.3, p = 0.001. 4.2.6. Task 6: facial expression of emotion: two-choice face–face expression matching There were overall differences in performance between HD patients and controls (U = 16.5, z = −2.9, p = 0.004) and between FTD patients and controls (U = 6.0, z = −3.8, p < 0.001) but not between HD and FTD patients. HD patients performed worse than controls for disgust (U = 18.0, z = −2.8, p = 0.004) and anger (U = 13.5, z = −3.1, p = 0.001). FTD performed more poorly than controls for sadness U = 21.0, z = −3.1, p = 0.002; disgust U = 0.0, z = −4.2, p < 0.001; anger U = 27.5, z = −2.6, p = 0.008. 4.2.7. Task 7: facial identity: two-choice face–face identity matching On this control task, involving matching faces for identity rather than emotion, there were no significant group differences. Both HD and FTD groups performed as well as controls. Moreover, the expressed emotion of the faces did not affect accuracy of identity matching.

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4.2.8. Task 8: vocal emotions: multiple-choice sound-label matching Group comparisons (Fig. 3(b)) showed overall group differences for surprise H = 7.7, p = 0.02; fear H = 12.5, p = 0.002; disgust H = 13.4, p = 0.001; anger H = 14.1, p = 0.001. The HD group performed more poorly than controls for three emotions only (fear U = 14.5, z = −3.0, p = 0.002; disgust U = 21.0, z = −2.8, p = 0.009; anger U = 15.5, z = −3.0, p = 0.003). The FTD group performed worse for all four emotions (surprise U = 24.5, z = −2.8, p = 0.005; fear U = 21.0, z = −3.0, p = 0.003; disgust U = 14.5, z = −3.5, p < 0.001; anger U = 13.5, z = −3.4, p = 0.001). The HD and FTD groups did not differ significantly on any emotion. Examination of emotions within each group showed that vocal emotions were not equally recognisable (control: 2r = 39.2, p < 0.001; HD: xr2 = 30.5, p < 0.001; FTD: 2r = 19.9, p = 0.001). For each group disgust was relatively well recognised and anger relatively poorly recognised. In the control group scores for disgust were significantly better than for all other emotions: happiness (z = −3.1, p = 0.002), surprise (z = −2.8, p = 0.005), sadness (z = −3.1, p = 0.002), fear (z = −2.7, p = 0.007), and anger (z = −3.1, p = 0.002). Scores for anger were significantly poorer than for surprise (z = −3.1 p = 0.002), fear (z = −2.7, p = 0.008), sadness (z = −2.8, p = 0.005), and disgust (z = −3.1, p = 0.002). In the patient groups a similar pattern pertained, although the superiority of disgust recognition was less pronounced. Scores for disgust in the HD group were significantly better than for anger (z = −2.7, p = 0.008) and fear (z = −2.5, p = 0.01). In the FTD group they were better than for anger only (z = −2.6, p = 0.01). A split half analysis showed comparable performance patterns for the two halves of the task. In both halves, disgust was most effectively recognised and anger least well recognised. Greatest impairments relative to controls were elicited in both patient groups for the emotions of fear, disgust and anger. No differences were elicited between the two patient groups. 4.2.9. Task 9: Manchester faces: expression recognition from full face Group comparisons (Fig. 3(c)) showed significant group differences for anger (H = 10.3, p = 0.006), disgust (H = 15.5, p < 0.001) and to a lesser extent surprise (H = 6.6, p = 0.04) and neutral faces (H = 6.6, p = 0.04). HD patients were poorer than controls in recognising anger (U = 18.0, z = −2.8, p = 0.005) and to a lesser extent disgust (U = 27.5, z = −2.3, p = 0.02). FTD patients were poorer than controls in recognising anger (U = 27.5, z = −2.6, p = 0.009), disgust (U = 10.0, z = −3.7, p < 0.001), surprise (U = 30.5, z = −2.5, p = 0.01), and neutral faces (U = 32.5, z = −2.3, p = 0.02). HD patients were better than FTD patients in recognising disgust (U = 29.5, z = −2.1, p = 0.04). Within group comparisons showed that emotions were not equally recognisable (controls: 2r = 25.0, p < 0.0001; FTD: 2r = 24.5, p < 0.001; HD: 2r = 15.5, p = 0.008). For each group happiness was best recognised, with scores being significantly superior (between p = 0.01 and 0.003) than for fear, surprise and anger, and in the case of FTD also than for disgust (z = −2.9, p = 0.004). In the control and HD groups recognition of disgust was not significantly poorer than any other emotion. 4.2.10. Task 10: Manchester faces: expression recognition from eyes only There were significant group differences only for the emotions of sadness (H = 8.4, p = 0.02), fear (H = 8.6, p = 0.01), and disgust (H = 10.4, p = 0.006). These reflected poorer performance in HD patients compared to controls for sadness (U = 29.5, z = −2.2, p = 0.03) and disgust (U = 15.5, z = −3.0, p = 0.002) and in FTD patients compared to controls for sadness (U = 27.0, z = −2.8,

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Fig. 4. Comparison of Ekman face data from this study (Sno) with that of Sprengelmeyer et al. (1996) (Spr) and Milders et al. (2003) (Mil). The figure shows mean group scores.

p = 0.005), fear (U = 26.0, z = −2.7, p = 0.007), and disgust (U = 30.5, z = −2.5, p = 0.01). HD and FTD patients did not differ significantly. Performance is shown in Fig. 3(d). Within group comparisons showed that for controls emotions were not equally recognisable from the eyes (2r = 16.6, p = 0.005). Sadness was significantly better recognised than surprise (z = −2.8, p = 0.005), anger (z = −2.9, p = 0.004) and disgust (z = −2.0, p = 0.05). For HD patients there was a minor difference only (H = 13.3, p = 0.02): superior recognition of sadness compared to anger (z = −2.4, p = 0.02). For FTD patients there was no difference in performance across emotions. 4.3. Relationship between emotion recognition and background neuropsychology The relationship between overall scores on the Ekman faces, sounds and Manchester faces tasks were compared and scores on background neuropsychological tests was examined for the three groups. In view of the multiple correlations significance was set at p < 0.01. No significant correlations were elicited for controls. In the HD group significant correlations were elicited only for letter fluency. By contrast, the FTD group showed significant correlations at the p < 0.01 level between emotion recognition scores and performance on each of the standard executive tests (WCST, Weigl’s, letter and category fluency, and Stroop) but not other neuropsychological measures. No significant correlation was elicited with scores on the Benton face test for any group. 4.4. Comparisons with other studies A direct comparison of HD data with those from Sprengelmeyer et al. (1996) and Milders et al. (2003) using the same test materials (Fig. 4) reveals largely similar performance across the three studies. Controls and patient groups are generally well matched in their level of performance for each emotion. However, there is a notable deviation with respect to disgust, there being a drop in test scores for the HD group in the Sprengelmeyer study. A comparison of FTD data with those from Keane et al. (2002) (Fig. 5(a) and (b)) shows a similar pattern of performance, the principle difference deviation being the greater impairment in facial recognition of fear demonstrated in the present study.

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Importantly, in both HD and FTD impairment was demonstrated across test modality (visual and auditory), providing support for claims that the problem is not simply one of recognising facial expressions (Keane et al., 2002; Sprengelmeyer et al., 1996), but rather reflects a multimodal impairment of emotion recognition. Emotion recognition deficits may contribute to patients’ difficulty in drawing inferences from social situations (Snowden et al., 2003) and HD patients’ tendency to misconstrue social interactions. FTD patients’ impairment in emotion recognition was generally more severe and pervasive than that of HD patients. Consistent with the findings of others (Keane et al., 2002; Lavenu et al., 1999) deficits in FTD were elicited across all emotions and there was no compelling evidence of selectivity of impairment. HD patients, as expected, showed impairment in the recognition of disgust. Nevertheless, in line with others (Milders et al., 2003; Montagne et al., 2006) they also showed notable impairment for fear and anger, a finding consistent across tasks. There was no evidence that the disgust recognition impairment was disproportionate to that relating to other emotions. Indeed, the greatest and most consistent impairment in HD patients was for the emotion of anger. This finding complements that of De Gelder, Van den Stock, De Diego Balaguer, and Bachoud-Levi (2008), which showed impaired recognition of angry body postures by HD patients. Anger impairment is, moreover, of clinical interest. Poor anger control is a characteristic feature of HD (Craufurd & Snowden, 2002). The impairment in recognition of anger suggests the possibility of parallel deficits in the production and reception of the emotion of anger. One might speculate too that a failure to recognise the expression of fear in others might be one factor that influences patients’ failure to modulate their angry behaviour in situations of interpersonal conflict. Impairments in fear and anger in addition to disgust are consistent with the known pathological involvement in HD of the striatum and amygdala (Mann et al., 1993). 5.1. Influence of task difficulty in HD

Fig. 5. Comparison of (a) Ekman facial expression and (b) emotion sound recognition data from this study (Sno) with that of Keane et al. (2002). The figure shows mean group scores.

5. Discussion The status of disgust recognition in HD is controversial. We sought to evaluate, through a comparative study of HD and FTD, the contrary claims of (a) disproportionate impairment in the recognition of disgust in HD and, (b) an absence of differences across emotions, performance being a product of task difficulty. As expected, both HD and FTD groups exhibited highly significant impairments in recognition of emotions compared to controls. Impairments in recognition of facial expression continued to be present when the mental demands of the task were minimised (two-choice tasks) and when verbal demands were eliminated (face–face-matching tasks), excluding explanations of impairment in terms of general mental demands or language. Performance on a control test of face identity matching was entirely normal, excluding an explanation in terms of impaired visual perception or attention. In keeping with the latter finding there was no correlation between emotion test performance and performance on the difficult Benton face perception test. The tests support the view that emotion recognition disturbance is a prominent feature of both HD and FTD.

Milders et al. (2003) argued, on the basis of their Ekman and Friesen face data, that the observed differences in expression recognition performance of their HD patients reflected differences in task difficulty rather than dysfunction of mechanisms dedicated to specific emotions. Indeed, the issue of differential difficulty of negative emotions has been raised outside the context of the HD literature (Adolphs, 2002). Our own Ekman face data, taken alone, might also invite a ‘level of difficulty’ account. The greatest and most consistent impairments in the patient groups occurred for the emotions of fear, disgust and anger, which were the three emotions on which control subjects performed most poorly. Nevertheless, other data challenge a task difficulty explanation. As predicted, the perceived difficulty of emotions by healthy controls varied according to the task. For example, whereas happiness was the emotion most easily recognised by controls in the full-face task (task 9), sadness was best recognised in the eye-only task (task 10). Although disgust was a difficult emotion in face tasks, it was the easiest emotion for controls in the sound task (task 8). Despite such changes in relative difficulty of emotions across tasks the pattern of impairment in the patient groups remained largely similar. It was not notably influenced by overall difficulty, as defined by control sample scores. Thus, in the sound recognition test, despite the facility of its recognition by controls, disgust continued to be impaired in the patient groups, in the case of HD patients along only with the emotions of fear and anger. For the Manchester face set, although surprise proved most difficult for controls, anger and disgust continued to be most impaired in the patient groups. For the Eyes-only task, although easiest for controls, the negative emotion of sadness elicited impairment in both patient

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groups. By contrast, although difficult to recognise by controls the positive emotion of surprise was not significantly impaired in either patient group. There appears to be a disproportionate difficulty for the HD group in recognising negative emotions, particularly of anger, fear and disgust, which cannot be accounted for simply by task difficulty. 5.2. Disgust impairment in HD: reconciliation of disparate results The findings point therefore to some selectivity in the breakdown of emotions in HD, in terms of negative emotions, but not to a specific disruption to disgust, as found by Sprengelmeyer et al. (1996, 1997). How can such disparities in findings be explained? Might the differences in finding be attributable to stage of illness? This would seem to be an unlikely explanation. Direct comparison of the present Ekman face data with those of Sprengelmeyer et al. (1996) reveals remarkably similar levels of HD performance for all emotions other than disgust. There is no evidence that patients in the present study were functioning at a generally lower level than those of Sprengelmeyer et al., to suggest a more advanced stage of illness. The control groups too performed similarly across studies, excluding the possibility that quirks in control performance influenced results. An alternative possibility is that differences in findings reflect heterogeneity within the HD population, some sub-groups showing disproportionate disgust recognition impairment and others not. Some support for the notion of individual differences comes from a voxel-based morphometric study of HD by Peinemann et al. (2005). Whereas group analysis showed robust volume changes in caudate and putamen, subgroup analysis showed variable degrees of insular atrophy, those HD patients with greatest insula atrophy performing poorest on executive tasks. Kipps, Duggins, McCusker, and Calder (2007) reported a strong correlation in HD patients between volume of the anteroventral insula and disgust recognition performance. While explanations in terms of clinical heterogeneity need to be borne in mind there was no clear support for this explanation in the present study. Examination of individual patient performance revealed no evidence of different performance profiles and no individual showed greater impairment for disgust than for other emotions. Moreover, a large cohort of HD patients and pre-symptomatic individuals (Johnson et al., 2007) failed to identify distinct sub-groups of patients with respect to their performance on emotion recognition tasks. Interestingly, the study by Kipps et al. (2007) failed to elicit a correlation between disgust recognition and structural change in the basal ganglia. Given that the striatum is the site of earliest and maximal pathology in HD it raises the question, even if there are individual differences in the magnitude of disgust recognition impairment, why disgust should be disproportionately affected relative to other emotions. A plausible alternative contribution to inconsistency of findings that requires consideration is response bias. A failure to detect a disproportionate impairment in disgust recognition in the present study might arise if patients favoured the ‘disgust’ response, thereby yielding a spuriously high number of correct responses in addition to false-positive errors. This possibility can be discounted, however, by the fact that error profiles were similar in the three groups. There was no evidence of abnormal response bias towards one emotion label in any group. It is of interest, however, that in all groups surprise was most often mistaken for fear and anger for disgust. Differences in response bias, across different HD studies, in favour of anger or disgust might feasibly ‘weight’ the relative magnitude of observed impairment for these two emotions, accounting for some differences in study findings. Substantial response biases would presumably have been noted and reported by the studies’ authors, so are unlikely to provide a sufficient

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account. It may be pertinent, however, that in studies that have demonstrated disproportionate impairment of disgust there is typically a general reduction in frequency of attribution of ‘disgust’ responses. This might reflect an inability to recognise disgust, in line with the authors’ interpretation. However, it raises the additional possibility that linguistic/conceptual factors might influence performance. Consideration of linguistic influences is particularly pertinent in the context of the conflicting findings in HD. The most consistent and compelling evidence of selective disgust impairment in HD has emerged from studies involving German speakers. Might, therefore, language affect results? Clues to the potential importance of language are present in the current study. Firstly, in task 2, HD patients were impaired in their ability to match the term ‘disgust’ with a situational context (task 2). This emotion label comprehension task was the sole task in which a selective impairment for disgust was elicited in the HD group. The findings are in keeping with those of Hayes, Stevenson, and Coltheart (2007) in suggesting that HD patients’ conceptual understanding of disgust may not be entirely normal. Secondly, in task 1, inter-rater reliability in classifying participants’ definitions of emotion terms was lowest for disgust. The basis for disagreement lay in the fact that whereas most emotion labels express a relatively specific, homogeneous affective state the term ‘disgust’ is applied in everyday parlance in a much broader range of contexts, covering moral indignation at unethical behaviour as well as repugnance at unpleasant sensory stimuli. The former has kinship with the emotion of anger, whereas the latter does not. The definitions provided by participants covered both moral and visceral interpretations, moral interpretations being the more common in all groups. It is noteworthy that the German word for disgust, “Ekel”, is not precisely equivalent in meaning to the English term “disgust”, ´ ut”. ˆ nor the French term “dego Whereas the French term, like the English, carries both moral and visceral connotations, the German term refers to visceral feelings alone. Disgust impairment might plausibly be more readily demonstrated in German-speaking patients by virtue of the greater purity/specificity of the disgust concept. Linguistic variations (and purity of concept) might not be confined to disgust. For example, the German term “Angst” conveys fear in the sense of the feeling of dread, whereas the term “Furcht” is more appropriately applied to a fear of something concrete. By contrast, the English word “fear” and the French word “peur” are applicable in both contexts. These potential sources of difference suggest that linguistic influences require further investigation. Disproportionate disgust impairments in HD (Sprengelmeyer et al., 1996, 1997, 2006) have been elicited thus far using tasks requiring matching an emotional stimulus (facial or vocal) with its corresponding verbal label. It would be important to establish whether comparable disproportionate impairments can be elicited using purely non-verbal tasks, such as the face–face matching of task 6. Equally, it would be important to disentangle, in English or French speaking populations, HD patients’ understanding of moral disapproval and sensory repugnance components of disgust. 5.3. Emotion recognition in FTD The findings in FTD are consistent with those of others (Keane et al., 2002; Lough et al., 2006) in showing widespread impairment in emotion recognition. Although most marked for negative emotions deficits extend to positive emotions including happiness. FTD patients were, moreover, significantly impaired, both in comparison with controls and HD patients, in their ability to assign the appropriate emotion label to a situational context. This suggests that impaired emotion recognition in FTD goes beyond the

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interpretation of sensory information to encompass conceptual aspects of emotion: knowing how one ought to feel according to the prevailing circumstances. Interpretation of emotion data in FTD requires a degree of caution. Unlike HD patients, for whom correlations with executive test performance were weak, FTD patients showed significant correlations between performance on emotion and standard executive tests, raising the possibility of an influence of general executive impairments on performance. Indeed, it may contribute to the lack of clear differentiation across emotions. Nevertheless, widespread deficits on emotion recognition tasks remained, even when executive demands of the task were reduced. Moreover, the absence of deficit on an identity-matching task, matched to the emotion-matching task in terms of executive demands, provides strong evidence that emotion recognition impairments in FTD are primary. 6. Conclusion The notion of selective disgust impairment in HD has acquired prominence in the emotion literature. The present study failed to corroborate the finding of disproportionate disgust impairment, greatest impairments being elicited for anger. The findings point to a need for caution in the automatic assumption of selective disgust impairment in HD. Nevertheless, the study elicited robust findings of impairment for fear, anger and disgust, which could not be accounted for by task difficulty, and suggest real differences in the processing and neural underpinning of negative, threatening emotions compared to positive emotions. The findings have clinical as well as theoretical relevance. Behavioural changes are the most challenging aspect of HD and FTD and create the greatest carer burden. Altered affect is a dominant source of breakdown in interpersonal relationships. Understanding the changes in emotion reception and expression in HD and FTD is crucial for patients’ management and support of their families. Acknowledgement We thank Dr. Jane Whittaker for permission to use the Manchester face sets. References Adolphs, R. (2002). Neural systems for recognizing emotion. Current Opinion in Neurobiology, 12(2), 169–177. Adolphs, R., Gosselin, F., Buchanan, T. W., Tranel, D., Schyns, P., & Damasio, A. R. (2005). A mechanism for impaired fear recognition after amygdala damage. Nature, 433, 68–72. Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. R. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature, 372, 669–672. Adolphs, R., Tranel, D., Damasio, H., & Damasio, A. R. (1995). Fear and the human amygdala. Journal of Neuroscience, 15, 5879–5891. Aylward, E. H., Codori, A. M., Rosenblatt, A., Sherr, M., Brandt, J., Stone, O. C., et al. (2000). Rate of caudate atrophy in presymptomatic and symptomatic stages of Huntington’s disease. Movement Disorder, 15, 552–560. Bathgate, D., Snowden, J. S., Varma, A., Blackshaw, A., & Neary, D. (2001). Behaviour in frontotemporal dementia, Alzheimer’s disease and vascular dementia. Acta Neurologica Scandinavica, 103, 367–378. Benton, A. L., Hemsher, K. S., Varney, N., & Spreen, O. (1983). Facial recognition test. In Contributions to neuropsychological assessment: A clinical manual. Oxford: Oxford University Press., pp. 30–43. Brandt, J. (1991). The Hopkins verbal learning test: Development of a new verbal memory test with six equivalent forms. The Clinical Neuropsychologist, 5, 125–142. Broks, P., Young, A. W., Maratos, E. J., Coffey, P. J., Calder, A. J., Isaac, C. L., et al. (1998). Face processing impairments after encephalitis: Amygdala damage and recognition of fear. Neuropsychologia, 36, 59–70. Calder, A. J., Keane, J., Lawrence, A. D., & Manes, F. (2004). Impaired recognition of anger following damage to the ventral striatum. Brain, 127, 1958–1969. Calder, A. J., Keane, J., Manes, F., Antoun, N., & Young, A. W. (2000). Impaired recognition and experience of disgust following brain injury. Nature Neuroscience, 3, 1077–1078.

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