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This article was submitted to Emotion Science, a section of the journal Frontiers in Psychology
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Huntington’s disease (HD) is a neurodegenerative movement disorder associated with deficits in the processing of emotional stimuli, including alterations in the self-reported subjective experience of emotion when presented with pictures of emotional scenes. The aim of this study was to determine whether individuals with HD, compared to unaffected controls, display abnormal visual scanning of emotionally evocative natural scenes. Using eye-tracking, we recorded eye-movements of 25 HD participants (advanced pre-symptomatic and early symptomatic) and 25 age-matched unaffected control participants during a picture viewing task. Participants viewed pictures of natural scenes associated with different emotions: anger, fear, disgust, happiness, or neutral, and evaluated those pictures on a valence rating scale. Individuals with HD displayed abnormal visual scanning patterns, but did not differ from controls with respect to their valence ratings. Specifically, compared to controls, HD participants spent less time fixating on the pictures and made longer scan paths. This finding highlights the importance of taking visual scanning behavior into account when investigating emotion processing in HD. The visual scanning patterns displayed by HD participants could reflect a heightened, but possibly unfocussed, search for information, and might be linked to attentional deficits or to altered subjective emotional experiences in HD. Another possibility is that HD participants may have found it more difficult than controls to evaluate the emotional valence of the scenes, and the heightened search for information was employed as a compensatory strategy.
Huntington’s disease (HD) is an autosomal dominant neurodegenerative movement disorder. Neural loss originates in the basal ganglia, and spreads progressively to a wide range of subcortical and cortical regions (
A large body of research indicates that people with HD have deficits in the processing of emotional stimuli, even prior to the onset of motor symptoms, i.e., in the pre-symptomatic phase of disease (c.f.,
Interestingly, findings regarding the self-reported experience of emotion vary depending on stimulus type. Studies using smells or verbal descriptions to induce an experience indicated diminished subjective experiences of disgust or fear in HD (
The purpose of the present study was to provide new insights into the processing of emotional stimuli in HD by addressing the question of whether people with HD show abnormalities in parameters characterizing global visual scanning behavior when viewing emotionally evocative natural scenes, compared to healthy control participants, as measured using eye-tracking. Visual scanning behavior was investigated for two reasons. Firstly, altered cognitive, emotional or motivational processes that take place during emotion processing in individuals with HD may influence visual scanning behavior and, therefore, observed alterations in scanning behavior in HD may be indicative of these processes. Considering the ambiguous self-report findings and the limits of asking individuals with HD to report on their own experience, the examination of eye-tracking parameters may add to a better understanding of how people with HD process emotionally evocative stimuli. Secondly, the altered evaluations of visual stimuli in HD may be caused by abnormal visual scanning. Specifically, visual scanning behavior affects the sensory information available for further processing during visual perception, and could therefore contribute to abnormal evaluations.
Eye-tracking enables us to identify parameters characterizing global visual scanning behavior. These parameters are related to the fixations and saccades made on a visual stimulus, and allow specific inferences regarding the processes taking place in the observer during visual perception. In particular, longer fixation durations typically indicate a deeper and more extensive processing of visual stimuli (e.g.,
The literature on HD offers several findings suggesting that the visual scanning of emotional scenes may be altered. Firstly, several previous eye-tracking studies in HD found alterations in visual scanning behavior during the completion of cognitive tasks, including tasks measuring attention (
In addition to research in HD, findings in Parkinson’s disease (PD) also raise the possibility that people with HD may show altered visual scanning of emotional scenes. PD is a motor disorder that shares similarities with HD in terms the affected neural circuitry and is associated with deficits in emotion processing similar to those present in HD (
In the present study, we recorded eye-movements and examined global visual scanning behavior during a picture viewing task that involved rating the emotional valence of natural scenes, and compared individuals with the gene-expansion for HD to control participants. We were interested in fixations as an indication of the depth of information processing. Therefore, we examined the portion of viewing time spent fixating on a visual scene, which is a function of the average duration and the number of fixations. We were also interested in saccades, as an indication of the extent of picture exploration. Specifically, we examined the scan path length, which is a function of the number of saccades and the average saccade length and can be interpreted as reflecting the degree of information seeking. Based on findings in HD showing deficits in the processing of emotional stimuli and abnormal visual scanning during cognitive tasks, and findings of altered visual scanning of emotionally evocative scenes in PD, we hypothesized that individuals with HD would show abnormalities in the duration and number of fixations, and with respect to length and number of saccades made when exploring the scenes. The complex array of previous findings related to the processing of emotional stimuli in HD, and the fact that eye-tracking research is sparse, made it difficult to make more specific predictions regarding how scanning patterns in HD may be altered. One possible prediction would be that altered processing of the emotional content of scenes in HD leads to abnormal scanning behavior. For example, exaggerated emotional experiences would be expected to result in long scan paths and frequent fixations, consistent with an enhanced search for information. Another possibility is that people with HD show altered visual scanning behavior due to disease-related changes in motivation or in motor and cognitive functioning, which could be reflected in self-report evaluations of emotional scenes due to different availability of visual information secondary to the scanning alternations. For example, people with HD, similar to people with PD, may show fewer fixations and longer scan paths than controls, maybe due to a lack of motivation. By contrast, a lack of differences between the HD and control groups in visual scanning would suggest that abnormal self-report evaluations of emotional scenes in HD are unlikely to result from altered visual scanning.
Twenty-five participants with the gene-expansion for HD and 25 healthy control participants took part in this study. Participants were recruited through local advertisement and participant databases. HD participants included pre-symptomatic and early symptomatic individuals that were genetically confirmed (CAG repeat length ≥ 39), expect for one symptomatic participant whose CAG status was indirectly verified by having a genetically confirmed offspring. The HD participants were included based on their Disease Burden Score (DBS;
Characteristics of study participants.
HD group | Control group | |||||||
---|---|---|---|---|---|---|---|---|
Mean | Min–Max | Mean | Min–Max | |||||
Age (years) | 49.4 | 8.8 | 36–67 | 25 | 49.6 | 8.9 | 35–66 | 25 |
Gender (F:M) | 14:11 | − | − | 25 | 15:10 | − | − | 25 |
Education (years) | 14.8 | 3.2 | 10–22 | 25 | 15.8 | 2.4 | 11–20 | 25 |
Handedness (R:L) | 23:2 | − | − | 25 | 22:3 | − | − | 25 |
AS | 13.6 | 5.7 | 4–33 | 25 | 11.4 | 7.2 | 0–30 | 25 |
QIDS 16 SR | 5.8 | 4 | 1–7 | 25 | 3.6 | 2 | 0–16 | 25 |
CAG repeat length | 43 | 1.5 | 40–47 | 24 | − | − | − | − |
DBS | 361 | 75.6 | 270–517 | 24 | − | − | − | − |
TFC score | 11 | 2.3 | 7–13 | 25 | − | − | − | − |
UHDRS motor score | 8.3 | 9.2 | 0–30 | 24 | − | − | − | − |
Diagnosed with symptomatic HD (Y:N) | 12:13 | − | − | 25 | − | − | − | − |
No HD related medication | − | |||||||
Medicated for depression | − | |||||||
Medicated for chorea | − |
During the picture viewing task, which was programmed using Presentation software (Neurobehavioral Systems, Inc., Berkeley, CA, USA), participants rested their head on a chin rest, at a distance of 80 cm from the display monitor (22-inch widescreen LCD monitor). The run-time of the task was around 30 min. Pictures of natural scenes (720 pixels × 576 pixels) were presented on a gray background in five randomized blocks (of 10 randomized stimuli), each associated with one of five emotions: anger, fear, disgust, happiness, and neutral. Thus, we used a total of 50 different images, including 10 images per emotion. Each trial consisted of the presentation of a fixation cross (for 0.5 s), a baseline screen (for 1 s), the scene stimulus (for 5 s), and finally a valence rating scale, which was shown until the participant responded via button press (
The images showed natural scenes involving objects, animals, landscapes, or interactions between people. We purposefully did not include any pictures showing close-ups of human faces since we were interested in the processing of scenes, rather than in facial emotion recognition. Natural scenes are unlikely to ever evoke only one singular emotion in the observer, yet we made an effort to select pictures for each emotion condition that would evoke the particular emotion predominantly. Most stimuli were taken from the IAPS (
Across the emotional conditions, we did not control for stimulus properties, such as brightness and spatial composition. Spatial composition is particularly relevant in the context of this study, as differences in the amount and distribution of details naturally influence scanning patterns, such as scan path length. For this reason, we did not have research questions related to differences between the emotions but presented some eye-tracking variables for each emotion individually, as well as combined, for illustrations purposes.
An EyeLink 1000 system (SR Research, Ottawa, ON, Canada) was used to record participants’ eye-movements binocularly at a sampling rate of 500 Hz. We calibrated and validated the eye-tracker at the start of the picture viewing task and in-between blocks. The eye-tracker automatically detected saccades based on the three default measures: amplitude of at least 0.1° visual angle, with a velocity of at least 30°/s, and with an acceleration of at least 8000°/s. Fixations were defined as periods without saccades. We analyzed the eye-tracking data for the right eye using the EyeLink Data Viewer (SR Research, Ottawa, ON, Canada). We excluded all trials with less than 50% screen viewing time, assuming that trials with strongly reduced screen viewing time, for example due to distraction, might be associated with abnormal viewing behavior (less than 10% of trails). For the saccade analysis, we excluded saccades that led to locations beyond the screen boundary, as those saccades are not part of the picture exploration.
For each trial, we extracted three fixation and three saccade parameters. Fixation parameters included: (1) the total fixation ratio (calculated as the total fixation duration divided by the trial viewing time, where trial viewing time was defined as the total trial time minus the time not spent viewing, for example due to blinks), which is a function of (2) the average fixation duration, and (3) the number of fixations. Saccade parameters included: (1) the scan path length in degree of visual angle (calculated as the sum of all saccade lengths), which consists of (2) the average saccade length in degree of visual angle, and (3) the number of saccades.
We used SPSS for Windows (IBM) to conduct statistical analyses. We analyzed the eye-tracking and rating data using analyses of variances (ANOVAs) and
To answer the question of whether HD and control participants differ in the portion of viewing time spent fixating on the scene stimuli, and to test whether possible group differences would differ between the emotional conditions, we analyzed the total fixation ratio using 2 × 5 repeated-measures ANOVAs with the factors Group (HD vs. control) and Emotion (anger, disgust, fear, happy, and neutral). We found that compared to control participants, the HD participants spent a significantly lower portion of viewing time fixating (
To further explain group differences in the total fixation ratio, we calculated
To answer the question of whether HD and control participants show differences in scan path length and to test for possible interactions with the emotional condition, we analyzed the scan path length using a 2 × 5 repeated-measures ANOVA with the factors Group (HD vs. control) and Emotion (anger, disgust, fear, happy, and neutral). We found that HD participants made longer scan paths compared to control participants (
To further explain group differences in the total scan path length, we calculated
We analyzed the valence ratings using a 2 × 5 repeated-measures ANOVA with the factors Group (HD vs. control) and Emotion (anger, disgust, fear, happy, and neutral). The results suggested that our stimuli were perceived in the expected way, without differences between HD and control participants (
Consistent with our hypothesis of abnormal fixation and saccade behavior during emotion processing in HD, we found that individuals with HD, compared to controls, spent a lower portion of picture viewing time fixating and made longer scan paths. These group differences occurred independent of the particular emotional content of the stimuli. The shorter fixation time was a result of shorter average fixation durations, rather than of a lower number of fixations. HD participants tended to make more fixations than controls, although the group difference was not statistically significant. The longer scan paths appeared to result from a combination of saccades that were somewhat more frequent and slightly longer; although group differences in these two parameters did not reach statistical significance.
Despite the altered visual scanning behavior in HD, we did not find group differences in the valence ratings of the stimuli, indicating that the abnormal scanning patterns did not affect the HD participants’ ability to extract the information necessary for performing those ratings, and that the participants in both groups experienced the valences of the stimuli similarly. A number of previous studies, however, have found altered self-reported emotional experiences in response to visual stimuli in individuals with HD (e.g.,
The visual scanning behavior we observed in the HD participants could reflect a heightened search for information, considering the long scan paths. Considering the short fixations, our findings may also indicate a shallow depth of information processing, i.e., unfocussed processing. The longer scan paths with shorter and somewhat more frequent fixations in our HD sample contrast with the shorter scan paths and fewer fixations that have been observed in PD patients compared to controls, who were studied during passive viewing of IAPS pictures (
A number of alternative explanations may account for the visual scanning patterns displayed by the HD participants in the current study. Some of these explanations relate to general deficits in HD and are not specific to emotion processing, whereas others are emotion-specific. Firstly, general physiological alterations in HD may play a role, considering that oculomotor abnormalities occur in HD, in particular slowed saccades and delayed saccade initiation (
Alternatively, an explanation for our findings that is specific to emotion processing, could be an exaggerated emotional experience, given that healthy individuals show longer scan paths and more frequent fixations for emotionally engaging IAPS scenes (
Finally, another emotion-related explanation for our observation of longer scan paths in HD participants, compared to controls, could be that the HD participants had difficulties evaluating the emotional valence of the stimuli, and a heightened search of information was employed in an attempt to compensate for these difficulties. Although it is reasonable to assume that cognitive impairment may have made it more difficult to evaluate the emotion-related elements of visual scenes, previous research suggests that the conceptual understanding of emotions remains relatively intact in HD, even in symptomatic individuals (
An important limitation of this study is the small participant sample, which is particularly relevant because of the variability in clinical phenotypes of HD. Additionally, future studies in HD could go beyond basic valence ratings as an indication of emotional experience, which may not be sensitive enough to detect group differences, thus potentially adding a richer set of data about the association of visual scanning behavior in HD with self-reported emotional experience.
Overall, this study found that HD participants displayed abnormalities in fixation and saccade behavior when processing the emotional content of natural scenes, which are consistent with enhanced, but possibly unfocussed, information seeking. These findings support previous self-report and neurophysiological studies suggesting altered processing of emotional visual stimuli in HD, and add an interesting element to understanding how emotion processing may be affected. This is the first investigation of visual scanning behavior for emotional visual scenes in HD, and although the results do not point to a singular explanation for the observed scanning behavior, they open up interesting questions for future research. We discussed a number of alternative explanations for the scanning patterns displayed by HD participants, including explanations that are not specific to emotion processing, such as physiological alterations and attentional problems, as well as emotion-specific explanations, such as an exaggerated emotional experience and difficulties evaluating emotional valence. Whether or not the observed effects are emotion-specific, our findings highlight the importance of taking visual scanning into account when investigating the processing of emotional scenes in HD, as altered scanning behavior may affect stimuli evaluations as well as their neural correlates.
CK conceptualized the study, collected, processed and analyzed the data, and prepared the manuscript. IL and JS contributed to the conceptualization of the study and critically revised and edited the manuscript.
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The authors offer their gratitude to all of the participants who volunteered to take part in this study.
IAPS pictures for happy were: 1460, 1604, 1610, 1630, 1710, 1920, 2388, 5001, 5779, 7330; IAPS pictures for disgust were: 7360, 7380, 9008, 9291, 9300, 9301, 9325, 9342, 9373, 9830; IAPS pictures for fear were: 1022, 1052, 1201, 1300, 1303, 1930, 1931, 5972, 6230, 7640; IAPS pictures for neutral were: 7004, 7009, 7010, 7012, 7021, 7025, 7052, 7081, 7179, 7235; Anger pictures included IAPS picture 2751, as well as depictions of acts of violence against animals or children, irresponsible behavior, such as littering or smoking in a car with children, and frustrating situations, such as a last minute flight cancelation at an airport. Anger pictures from the internet where chosen through a small pilot study where lab members were asked to categorize preselected images.