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Altered subjective fear responses in Huntington’s disease

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Abstract

Patients with Huntington’s disease (HD) have been shown to exhibit impairment in the recognition of facial expressions such as disgust, as well as deficits in disgust responses to olfactory and gustatory stimuli. The present study investigated whether HD is associated with changes in emotional responses to a variety of visual and verbal stimuli selected to elicit core disgust, moral disgust, fear and happiness. Thirteen patients with HD and twelve controls provided emotional ratings after both reading emotion eliciting scenarios and viewing pictures from the International Affective Picture System database. Patients with HD exhibited executive dysfunction. In comparison to controls, they gave similar ratings for happy stimuli and did not differ significantly in response to core disgust or moral disgust stimuli. However, they did exhibit lower fear ratings in response to both sets of fear stimuli (pictures and scenarios), and higher anger ratings than controls in response to fear pictures. These differences in fear response could reflect dysfunction within frontostriatal pathways involving the amygdala. Changes to fear responses in HD may impair decision making and lead to increased risk-taking behaviour with significant personal or social consequences.

Introduction

Patients with Huntington’s disease (HD) demonstrate impairments in recognising facial expressions of disgust [1]. The characteristic facial expression of disgust involves constriction of the mouth and nose, signalling resistance to ingestion. Core disgust is typically experienced in response to an unpleasant taste or smell, is associated with nausea, and has been linked to the insula [2], a neural region critical for the awareness of bodily sensations. Core disgust enables organisms to avoid harmful contact with potential contaminants such as rotting food or body products. Disgust deficits have been revealed in HD using pictures, olfactory and gustatory stimuli [3]. Snowden et al. [4] showed that patients with HD can exhibit poor recognition of vocally expressed disgust and reduced disgust responses in response to written scenarios that elicited this emotion in control participants.

While some authors argue difficulties with disgust are disproportionate compared to recognition of other emotional expressions [1], [3], studies have revealed deficits in the recognition of a range of negative emotional facial expressions in HD [5] and one study found greater impairment in the recognition of fearful facial expressions [6]. However, it is generally assumed that positive emotions including happiness are unaffected.

Sprengelmeyer et al. [7] showed that poor recognition of fearful facial expressions was accompanied by reductions in two HD patients’ emotional experience of fear. This may be because the neural regions involved in emotion recognition in others are implicated in the experience of that emotion [2]. As patients with HD exhibit difficulties recognising certain emotions, their subjective experience of those emotions may differ to neurologically intact individuals. The current study therefore aimed to assess a range of emotional reactions of patients with HD, through the use of stimuli associated with fear and disgust.

One complication when investigating the experience of disgust lies in the range of stimuli that elicit this emotion. For example, disgust may be elicited by some moral (e.g. antisocial or criminal) offences [8]. While many previous investigations have focused on core disgust, the current study may be the first to investigate moral disgust in patients with HD.

Previous research investigating emotional processing in HD mainly focused on patients’ recognition of emotional facial expressions, with limited attention to whether changes in one’s own emotional experience were a feature of HD. For example, it could be that changes in the recognition of others’ disgust are accompanied by changes in the experience of disgust in HD. We investigated subjective emotional responses to pictures and scenarios selected to elicit core disgust, moral disgust, fear and happiness, comparing patients with clinical HD to healthy controls. It was expected that patients with HD would show reduced disgust responses to both core and moral disgust stimuli, and to a lesser extent reduced fear responses to fear stimuli, but that reactions to happiness stimuli would be unaffected.

Section snippets

Methods

This study was granted ethical approval by a local Ethics Committee. All participants gave written informed consent.

Results

Patients and controls did not differ significantly for age or education.

Discussion

We report evidence of altered subjective fear responses in HD. Patients with HD were similar to controls in that they rated the target emotions for each emotional category higher than other emotions. However, there were significant differences between the groups for fear pictures and scenarios. Patients gave lower fear ratings than controls for pictures and scenarios selected to elicit this emotion. They also gave higher anger ratings in response to fear pictures.

Patients with HD gave lower

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    Interestingly, our finding of reduced facial muscle responsivity to disgusting scenes in HD contradicts previous self-report studies, which have not found diminished disgust experiences to emotionally-evocative scenes. In fact, self-report studies have most commonly indicated exaggerated responsivity of various emotional states in response to scenes (De Tommaso et al., 2013; Eddy et al., 2011; Ille, Holl, et al., 2011; Paradiso et al., 2008), including a higher intensity of disgust experience in one study (Ille, Holl, et al., 2011). The difference between our study and the previous findings may be because we measured spontaneous muscle activity using EMG, which, unlike self-report, does not require the interpretation of one's own experience.

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    In contrast to studies using tastes and smells to evoke emotional experiences, studies using pictures of scenes found more evidence for exaggerated, rather than diminished, experiences of several emotional states, including disgust. Specifically, five studies compared symptomatic HD participants to healthy control participants (De Tommaso et al., 2013; Eddy et al., 2011; Ille et al., 2011a, b; Paradiso et al., 2008), and a diminished emotional experience was only observed in one study and only for fear (Eddy et al., 2011). These authors examined fear, happiness, core disgust, and moral disgust, and HD participants reported lower fear, but higher anger, in response to fear-inducing scenes than control participants.

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The review of this paper was entirely handled by an Associate Editor, Dr. V. Bonifati.

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