The aim of this study was to explore whether the response time, as a proxy of the readiness of the motor system, in discriminating emotional stimuli differed among different types of stimuli, characterized by the presence or not of embodiment in patients with early-stage PD. To this aim we investigated motor readiness when processing embodied (emotional body language [EBL] and emotional facial expressions [FACS]) vs non-embodied (emotional scenes [IAPS]) stimuli with neutral, happy, and fearful content.
The key findings are as follows: (i) Overall, individuals with PD displayed longer response times than healthy controls (HC) when discriminating both fearful ('Fear') and happy ('Happiness') stimuli.; (ii) In both PD and HC groups, when distinguishing 'Happiness' from non-emotional ('Neutral') stimuli, response times were prolonged when discriminating Emotional Body Language (EBL) in comparison to Facial Action Coding System (FACS) and International Affective Picture System (IAPS) stimuli; (iii) In HC, when distinguishing 'Fear' in contrast to 'Neutral' stimuli, response times were longer for EBL when compared to FACS and IAPS stimuli. However, in individuals with PD, while discriminating 'Fear' versus 'Neutral' stimuli, response times were longer when discriminating EBL only in comparison to FACS but not when compared to IAPS; (iv) Specifically in individuals with PD, when distinguishing 'Fear' stimuli versus 'Neutral' stimuli, response times were shorter for FACS compared to IAPS;(v) In individuals with PD, response times for discriminating fearful EBL stimuli exhibited a significant correlation with sub-items 3.2 and 3.13 of the MDS-UPDRS III, which pertain to 'facial expression' and 'posture,' respectively.
First, longer RTs in PD in all sets of pictures (‘Fear’ and ‘Happiness’), compared to HC may be ascribed to one of the main symptoms in PD, which is bradykinesia.
In terms of the emotional aspects of the stimuli, both the PD and HC groups exhibited comparable behaviour when exposed to stimuli associated with 'Happiness.' In both cases, they displayed longer RTs when distinguishing between EBL in comparison to IAPS and the FACS stimuli, with no significant difference observed between the latter two.. This outcome aligns with our prior research, which examined RTs in distinguishing EBL in relation to IAPS [9] and can be attributed to the characteristics of the stimuli. One potential interpretation for this result could be that the information conveyed by the arms and hands in EBL, which play a crucial role in accurately processing certain specific emotions [19],[20], are ambiguous in happy images. A closed fist, that is often present in ‘Happiness’ EBL stimuli, might be an indication of anger [19],[21], and hence, it might results in longer times for correctly interpreting the observed body posture. Given that the hands demand more attentional resources when interpreting the emotions conveyed through body language, and considering that our happy stimuli predominantly featured actors with closed fists in cheerful postures like jubilation or exultation, it is reasonable to speculate that the prolonged response times observed in the 'Happy' condition could be attributed to this incongruence between the body posture and hand gestures.
Differences between individuals with PD and HC emerged during the discrimination task involving 'Fear' stimuli. Our findings indicate that individuals with PD exhibit accelerated motor responses when faced with potential threats, as represented by fearful stimuli in the embodied set. This heightened response speed in PD led to no significant differences in RTs when distinguishing 'Fear' EBL stimuli from 'Fear' IAPS stimuli, and even faster responses when discriminating between 'Fear' FACS stimuli from 'Fear' IAPS stimuli, in contrast to the responses of HC. Alternatively, we can also interpret our data as suggesting that individuals with PD may have difficulty in discerning 'Fear' IAPS stimuli, as their reaction times for these stimuli were longer compared to the reaction times for 'Fear' FACS, and comparable to the ones for 'Fear' EBL stimuli. However, this explanation is less likely, given that the analysis of valence scores did not reveal any significant PICTURE*GROUP interaction, indicating a similar ability for individuals with PD and HC in recognizing emotions across the three sets of stimuli. It's important to highlight that, similar to our earlier study [9], we specifically chose IAPS stimuli for the 'Fear' condition from a limited pool of images known to predominantly elicit fear, such as those depicting human attacks and accidents[22]. Secondly, in order to eliminate the majority of body movement cues, we made the deliberate choice to exclude any IAPS images showing entire human bodies engaged in actions. This decision ensured that we had a suitable set of images for direct comparison with the 'embodied' stimulus sets, namely FACS and EBL.
From our findings we can infer that embodied stimuli representing fear (i) are more rapidly processed in PD OR (ii) may induce a faster motor response in the discrimination task.
Related to the first hypothesis, there are data in the literature on early emotion processing in PD collected by means of event-related potentials (ERPs) [23]. Results showed that pictures of high compared to low emotional arousal were associated with a pronounced relative negative shift in the ERP waveform over parietal and occipital sites developing about 220 ms after picture onset. This early posterior negativity (EPN) did not differ between PD and control group, suggesting early emotion processing in PD is comparable to controls. In a subsequent work the authors investigated EPN in response to emotional compared to neutral facial expressions (angry, fearful, disgusted, sad, and happy) [24]. Results showed that in control subjects, the EPN of the ERP, which is thought to reflect early perceptual emotion discrimination, was larger in response to emotional compared to neutral facial expressions. In contrast, this emotional modulation of the EPN was absent in PD patients indicating impaired early emotion discrimination. Noteworthy, any difference was found related to latency of EPN, reflecting a processing time comparable between PD and controls. Taking into consideration these data, we consider unlikely that our results may be the consequence of faster processing of emotional stimuli. Indeed, our findings are specific to ‘Fear’ embodied stimuli, whereas ERP data indicated impaired early emotion discrimination for all emotional face expression. Furthermore, we found here a gain of performance in discriminating ‘Fear’ embodied stimuli and not the opposite.
Regarding the second hypothesis, i.e., that embodied stimuli representing fear induce a faster motor response in the discrimination task, we can discuss this hypothesis considering the effect that emotional stimuli exert on motor function in PD. In PD, it has been described since many years the ‘kinesia paradoxa’ phenomenon, defined as “the sudden transient ability of a patient with PD to perform a task he or she was previously unable to perform” [25]. Various theories have been developed to explain this phenomenon ranging from noradrenergic activation to activation of alternative motor pathways with respect to those normally activated during voluntary movement under non-emotional circumstances [26]. Particularly, activation of the limbic circuit of the basal ganglia, one of the multiple and segregated cortico-subcortical-cortical pathways involving the basal ganglia [27], has been proposed [2].
Hence, we can speculate that the ‘Fear’ embodied stimuli may induce a switch to the emotional basal ganglion module, making motor response (here, response times) faster.
This alternative ‘emotional’ motor pathway can play a compensatory role in PD to counteract dysfunctions induced by dopaminergic deficit in other basal ganglia motor pathways, making the motor aspects in PD so sensible to emotional distress [2]. The effectiveness of these affective compensatory mechanisms might be suggested by the negative correlations we found between RTs in discriminating ‘Fear’ EBL stimuli and the two MDS-UPDRS III subitems investigating facial mimicry and posture, apparently making the EBL set of stimuli particularly sensible to test motor readiness in response to emotional stimuli, possibly because of the amount of motor information conveyed by this set of stimuli.
Based on these results, we can speculate that PD patients with more severe axial symptoms are apparently more able to call into action the compensatory ‘emotional’ motor pathway compared to patients with less symptoms, especially when it comes to threatening stimuli processing. Following this line of reasoning we can also speculate that lost in this compensation may be responsible of worsening of motor symptoms as in the case of freezing of gait (FOG), that is largely sensible of emotional distress with worsening of FOG symptoms in relation to anxiety [3].
Here, we recruited patients in their early clinical stage (phases 1 and 2 of Hoehn and Yahr scale) and no one experienced FOG. Following a hypothesis implying the loss of compensation of emotional alternative pathway in PD with FOG, RTs when discriminating ‘Fear’ embodied stimuli are not supposed to be speeded up in FOG patients, due to the loss of compensatory activity in the emotional alternative pathway. It would be interesting address this hypothesis in future studies.
Some limitations of the present study should be considered. First, the experiment was conducted on-line and no direct monitoring from the experimenter was available. However, results were consistent, and outliers were excluded from the analysis. Second, this study included only patients in the early stage of the disease and to include patients in a more advanced stage (also with FOG) is required to confirm our hypothesis on the relation between RTs modulation with ‘Fear’ embodied stimuli and motor symptoms worsening.
In summary, we have demonstrated that in the context of a discrimination task involving 'Fear' embodied stimuli (FACS and EBL), motor responses were notably quicker in PD patients. This observation is substantiated by the shorter reaction times (RTs) for FACS compared to IAPS and the absence of a significant RT difference, despite the variance in complexity, for EBL in comparison to IAPS. We have put forth hypotheses regarding potential mechanisms that could underlie the engagement of an alternative emotional motor pathway, contributing to improved motor performance during 'Fear' processing.