Dottorato in NEUROSCIENZE CLINICO-SPERIMENTALI E PSICHIATRIA

Titolo della tesi: Emotion recognition in Amyotrophic Lateral Sclerosis in the dynamic environment

Background and aims: Although traditionally characterized as a pure motor system disorder, ALS is now recognized to affect multiple systems, with cognitive impairment representing the most frequent non-motor symptom. ALS patients may have deficit in executive functions, behavioral impairment, anomalies in emotion processing and social cognition. The construct of social cognition represents the set of cognitive processes used to encode, decode, store, retrieve and use information about people in social relationships. A key aspect of social cognition is the ability to infer other people's mental states (i.e. beliefs, preferences and intentions), thoughts and feelings; it is referred to as “theory of mind” (ToM). ALS seems to be associated with significant impairment in facial emotion recognition, especially for disgust and surprise, as assessed by static test. Nevertheless, the previous studies directly investigating ToM abilities in ALS patients have provided heterogeneous results. The aim of our study was to measure the ability of ALS patients to process dynamic facial expressions as compared to a control group of healthy subjects and to correlate this ability in ALS patients with neuropsychological, clinical and neurological measures of the disease such as the Edimburgh Cognitive ALS Screen (ECAS) test, a limb/bulbar onset phenotype, age, disease duration, education level, the Medical Research Scale (MRC) muscle scale, the ALS Functional Rating Scale - Revised (ALSFRS-R). Materials and methods: This is a single center cross-sectional study conducted in the Rare Neuromuscular Disorders Unit of the Umberto I University Hospital, Sapienza University of Rome, Italy. Sixty-three subjects affected by ALS, without non ALS-specific cognitive disorders at the ECAS test, and 47 healthy controls were recruited between January 2017 and December 2020. We recorded the following baseline data: age, disease duration, sex, education level. All the ALS patients enrolled in the study also underwent i) the Geneva Emotion Recognition Test (GERT) in which ten actors express 14 types of dynamic emotions in brief video clips with audio, ii) the ECAS test; iii) the ALSFRS-R and iv) the MRC for the evaluation of muscle strength. All the healthy subjects enrolled in the study underwent the GERT. The correctly recognized emotions in the ALS group were compared to the control group. False recognitions in the ALS group versus control group were also compared. Results: The two groups were well matched for age and level of education. Overall, the percentage of true and false emotion recognition were similar in the two groups (respectively 36,47% in ALS versus 39,16% in the control group and 66,00% in ALS versus 62,07% in the control group). When considering individual emotions, the recognition of irritation and pleasure was significantly different between ALS patients and the control group. The amusement, despair, irritation, joy, sadness and surprise had been falsely recognized differently between ALS patients and the control group. Specific ALS cognitive impairment was associated with bulbar-onset phenotype (OR=14,3889; 95%CI=3,96-52,16); it was not associated with age (F(1,61)=2,2761, p=0,13672), disease duration ((F(1,61)=1,0920, p=0,30186) or schooling (F(1,61)=0,35300, p=0,55481). The number of recognition mistakes was related to age (F=11.479; p=0,001). It was not related to the duration of disease (F=2.358; p=0,131), neither to the MRC muscle scale (F=1,868; p=0,179), neither to the ALSFRS.R total score (F=0,686; p=0,412), neither to the education level (F=3,178; p=0,08). No association was observed between false emotion recognition and cognitive impairment (F(1,60)=,56971, p=,45333) The number of categorical errors was significantly higher in the ALS patients than in the control group (27,66±7,28 vs 17,72±5,29; t=8,723; p=0.001) (Fig. 10). In particular, ALS patients committed a greater number of errors in quadrants different from the macro-categories compared to the control group (27,66±7,28 vs 16,72±5,29; t=8,723; p=0,0001) . Furthermore, in the first months after disease diagnosis, the recognition of emotions seems to be independent of the cognitive impairment, while subsequently there is a trend towards the reduction of the recognition of emotions in the cognitively impaired group compared to the cognitively healthy group Conclusions: patients with ALS show deficits in the dynamic processing of a wide range of emotions, different than previously detected. It is possible that this discrepancy is justified by the different techniques used in our study, static versus dynamic evaluations. At the same time, these deficits are not necessarily associated with a decline in higher cognitive functions: this could therefore lead to an underestimation of the phenomenon and a lack of consideration of aspects that should instead be analyzed in the context of neurodegenerative and rapidly progressive diseases such as ALS. The potential clinical implications of social cognition impairment in patients with classic ALS have major importance. Problems with judgment, attention, inhibition, and generation of responses should be taken into account when patient care is planned as it may compromise capacity to make decisions about health care or financial circumstances, and the ability to engage competently in end-of-life decisions.