Introversion and Neuroticism in Akinetic-Rigid Parkinson’s Disease: Association With Frontal-Executive Dysfunction

Personality characteristics are distinctive and recurrent patterns of thoughts, feelings, and actions that occur in response to particular situational demands (1). Personality characteristics such as anxiety proneness, introversion, low response to novelty, cautiousness, and rigidity may represent early manifestations of Parkinson’s disease (PD) (2, 3). PD is a neurodegenerative disorder characterized by motor and nonmotor symptoms arising from degeneration of the nigrostriatal pathway and interconnected neurotransmitter systems (4). Investigators who have explored the personality profiles of people with PD have often reported similar findings, notwithstanding the different personality models used in their exploration. In studies based on Eysenck’s personality model (5), investigators have observed that neuroticism was the predominant trait in PD (6, 7). Eysenck’s model (5, 8) includes three personality dimensions: extraversion, defined as the degree to which a person is outgoing and interactive with other people; neuroticism, defined as an increased tendency to emotional reactivity; and psychoticism, referring to an underlying predisposition of personality to develop anomalies of a psychiatric nature. Some authors (6) observed that neuroticism and introversion increased the risk for PD. Other authors (7) showed that neuroticism and extraversion personality traits were associated with worse quality of life among people with PD. Thus, these findings highlight the necessity to develop specific approaches to improve daily living function for those with PD, especially during the treatment process. Similar findings were found in studies based on the Big Five personality traits model (9, 10). Indeed, patients with early PD showed high neuroticism and conscientiousness and low extraversion, excitement, seeking, and openness to ideas compared with healthy participants (11–13). Studies based on Cloninger’s psychobiological model (14) described the temperament of people with PD as characterized by low novelty seeking (e.g., the tendency to respond to novelty, danger, and the cue for reward) and high harm avoidance (e.g., the tendency to avoid adverse stimuli) (15, 16). Recent studies (3, 17, 18) also support the concept of “Parkinsonian personality,” characterized by clinical features similar to those of obsessive-compulsive personality disorder, featuring a chronic, pervasive, and maladaptive pattern of preoccupation with orderliness, perfectionism, and mental and interpretative control at the expense of flexibility, openness, and efficiency (19).

However, although it seems clear that particular personality traits characterize people with PD, only a few studies have explored the potential psychological mechanisms underlying these clinic manifestations. Volpato et al. (13) observed among people with PD and no dementia that the personality dimension of emotional stability (characterized by the ability to control emotional reactions and the absence of negative effects, such as anxiety or depression) was associated with planning dysfunction and that the personality dimension of openness to experience (characterized by cultural interests, creativity, curiosity, and openness toward new and different values and cultures) was associated with cognitive flexibility dysfunction. However, these investigators performed assessments of a restricted set of frontal-executive functions and did not explore the possible contribution of selective and sustained attention or the role of inhibitory control processes. Another group of investigators (20) reported that the personality dimension of reward dependence ( the tendency to actively react to rewards) was correlated with dysfunction of cognitive flexibility and that the personality dimension of persistence (perseverance despite frustration and fatigue) was associated with impairments in divergent thinking and inhibitory control among people with PD and no dementia. However, although these authors investigated the contribution of the frontal-executive functions, other cognitive abilities, such as anterograde memory or visuospatial skills, were not explored. Luca et al. (21) also focused on the involvement of general frontal-executive function in the personality dimension of harm avoidance (the tendency to avoid aversive stimuli) among people with PD and no dementia. Taken together, these studies investigated only the correlations between personality traits and frontal function among people with PD without examining complex interactions with the specific motor characteristics of the disease. Indeed, PD has often been described as a heterogeneous neurodegenerative disorder characterized by tremor, rigidity, and other motor symptoms, each associated with a specific disease course and treatment response (22).

Interestingly, some investigators more recently found that people with PD who showed freezing of gait had lower levels of extraversion and higher levels of neuroticism than those with PD who did not show freezing of gait (23). Moreover, other authors observed strong correlations between anxiety symptoms and onset of freezing of gait (24) and between high novelty seeking and low self-directedness (23) in people with PD. Taken together, these findings seem to suggest that specific personality traits could be common among individuals with different motor subtypes of PD and that these personality traits could be associated with specific frontal-executive dysfunction. To the best of our knowledge, no study has evaluated the correlation between personality and cognitive function, especially frontal function, across individuals with different motor subtypes of PD.

In the present study, we assessed a prospective sample of people with PD to investigate whether personality traits were associated with a specific motor subtype of PD (tremor-dominant or akinetic-rigid phenotype) and whether specific aspects of frontal-executive function were associated with the personality traits of people with either the tremor-dominant or the akinetic-rigid motor subtype of PD. We discovered that people with PD with the akinetic-rigid subtype showed higher levels of neuroticism and introversion than those with the tremor-dominant subtype. Moreover, the associations between frontal-executive dysfunction were stronger in people with the akinetic-rigid subtype of PD. These findings expand the clinical characterization of people with PD by providing novel insights into the relationships among the different clinical features of the disease.

Methods

Participants

People with PD were selected from an outpatient population attending the movement disorders unit of the University of Naples Federico II. Patient data were collected between April 2021 and November 2021. To be eligible for participation in this study, patients had to have a clinical diagnosis of PD according to Movement Disorder Society clinical diagnostic criteria (4) and had to be taking an antiparkinsonian treatment at a stable daily dosage.

Among people with PD, 41 patients (men, N=24) satisfied the inclusion criteria (mean±SD age was 65.4±7.7 years; mean education level was 10±3.9 years). This sample was composed of Caucasian individuals (100% Italian). The participants did not show major neurocognitive disorder (19) or moderate to severe cognitive decline (as expressed by an age- and education-adjusted score below normal range based on the Italian validation of the Mini-Mental State Examination [MMSE]) (25). Motor symptoms were assessed at onset of the disease with the motor subscale of the Unified Parkinson’s Disease Rating Scale (UPDRS-III) (26); disease stage was assessed with the Hoehn and Yahr scale (27) in the off state. At the time of testing, participants were receiving either levodopa (l-DOPA) or dopamine agonist treatment, and no participants were being treated with advanced therapies. Forty healthy control participants (men, N=19) who were Caucasian (100% Italian), were similar in age and education level to the PD sample (age: t=1.457, df=1, p=0.14; education level: t=0.029, df=1, p=0.97), and had no previous history of neurological or psychiatric disease were recruited from elderly volunteer associations and agreed to participate in the study.

The study was approved by the ethics committee of the University of Naples Federico II and conducted in accordance with the ethical standards of the Helsinki Declaration. All participants provided written informed consent to participate in the study.

Assessment of Cognitive Abilities

All participants completed a neuropsychological battery, which included Italian versions of the following assessment tools: MMSE, Montreal Cognitive Assessment (MOCA), Corsi span forward test, figure copying test, bisyllabic word repetition, immediate and delayed recall on the Auditory Verbal Learning Test, Frontal Assessment Battery, phonological verbal fluency test, attentional matrices, Trail-Making Test, Stroop Color and Word Test, and Symbol Digit Modalities Test. The classification of tests according to the specific cognitive domains explored, with corresponding references, is summarized in Table 1 (28–34).

Assessment of Psychological Features and Personality Traits

All participants completed a psychological assessment that included the following inventory and scales: the Beck Depression Inventory–Second Edition (BDI-II), the 90-item Symptom Checklist–Revised (SCL-90-R), and the Emotional Inhibition Scale (EIS). Moreover, all participants completed the Eysenck Personality Questionnaire–Revised (EPQ-R) as an assessment of personality traits. A detailed description of these instruments, with corresponding references, is summarized in Table 1 (5, 35–37).

Statistical Analysis

To identify PD motor subtypes, we used the classification method by Kang et al. (38) to categorize people with PD in the following three groups: tremor-dominant, mixed, and akinetic-rigid groups. The ratio of the mean UPDRS tremor-dominant score (sum of scores for UPDRS-III items 20 and 21 divided by four) to the mean UPDRS akinetic-rigid score (sum of scores for UPDRS-III items 22–27 and 31 divided by 15) was used to identify people with tremor-dominant PD (ratio >1), mixed PD (0.8≤ratio≤1.0), and akinetic-rigid PD (ratio <0.8). Then, the group of healthy control participants and groups of participants with particular motor subtypes of PD were compared based on demographic characteristics (age and education); clinical characteristics (disease duration, l-DOPA equivalent daily dosage, UPDRS-III score, and Hoehn and Yahr scale stage); and cognitive, psychological, and personality test scores. For this purpose, we ran separate multivariate analyses of variance (MANOVAs) by entering the diagnosis (healthy control participants, tremor-dominant PD, and akinetic-rigid PD) as a between-subjects factor and the cognitive, psychological, or personality test scores as dependent variables in each model. Post hoc analyses were performed by using the Bonferroni test, setting the level of significance at a p value <0.05.

Moreover, to explore the possible association between specific cognitive abilities and personality traits among people with a specific motor subtype of PD (tremor-dominant PD, mixed PD, and akinetic-rigid PD), we computed Pearson’s correlation coefficients between the raw scores on the variables considered in each PD subtype separately. All data analyses were performed by using SPSS Statistics, version 24.0.

Results

No healthy participants exhibited motor symptoms. Among the 41 people with PD, 20 (48.8%) people exhibited the tremor-dominant phenotype of PD, whereas 21 (51.2%) people exhibited the akinetic-rigid phenotype of PD. No participant with PD manifested the mixed motor subtype of PD. Data on demographic and clinical features and cognitive, psychological, and personality test scores are summarized in Table 2.

MANOVAs were used to compare demographic and clinical features and performance on cognitive tests and showed a main effect of diagnosis (Wilks’ λ=0.12, df=2, p<0.001; η²_p=0.64). When compared with the healthy control group, the tremor-dominant and akinetic-rigid PD groups achieved significantly poorer scores on the MMSE; MOCA; immediate and delayed recall on the Auditory Verbal Learning Test; Frontal Assessment Battery; phonological verbal fluency; attentional matrices; Trail-Making Test, part A (time) and part B (accuracy and time), and Trail-Making Test, parts B–A; Stroop Color and Word Test (errors and time); and Symbol Digit Modalities Test (all comparisons were adjusted by using the Bonferroni test: p<0.001). Moreover, participants in the akinetic-rigid PD group scored significantly lower than those in the tremor-dominant PD group on the Frontal Assessment Battery (p=0.008), Trail-Making Test, part B (accuracy: p=0.04; time: p=0.04), and Trail-Making Test, parts B–A (accuracy: p=0.04; time: p=0.03), and significantly lower than the healthy control participants on the figure copying test (p=0.04). No significant differences were found among the healthy control, tremor-dominant PD, and akinetic-rigid PD groups on the Corsi span forward test and bisyllabic word repetition.

MANOVAs were used to compare psychological test scores (Table 3) and showed a main effect of diagnosis (Wilks’ λ=0.07, df=2, p<0.001; η²_p=0.72). In particular, the akinetic-rigid PD group, compared with the healthy control group, scored significantly higher on the BDI-II (cognitive component, p=0.01; somatic-affective component, p=0.02; general depression level, p=0.008), the SCL-90-R (somatization, p<0.005; obsessive-compulsive, p<0.005; interpersonal sensitivity, p<0.005; depression, p<0.005; anxiety, p<0.005; hostility, p<0.005; paranoid ideation, p<0.005; psychoticism, p<0.005), and the EIS (timidity, p=0.04; self-control, p=0.03). Interestingly, compared with the tremor-dominant PD group, the akinetic-rigid PD group had higher scores on individual items of the SCL-90-R, including the obsessive-compulsive (p<0.02), depression (p<0.03), anxiety (p<0.02), paranoid ideation (p<0.04), and psychoticism (p<0.04) subscales, resulting in a higher total score (p<0.001).

MANOVAs were used to compare the scores on personality traits tests (Table 3) and were statistically significant (Wilks’ λ=0.25, df=2, p<0.001; η²_p=0.49). When compared with the healthy control group, the akinetic-rigid PD group scored significantly higher on the neuroticism subscale (p<0.001) and on the extraversion subscale (p<0.001) of the EPQ-R. Moreover, when compared with the tremor-dominant PD group, the akinetic-rigid PD group achieved significantly higher scores on the neuroticism subscale (p<0.001) and lower scores on the extraversion subscale (p=0.007) of the EPQ-R. No significant differences among groups were found on the psychoticism subscale. Furthermore, the tremor-dominant PD group exhibited significantly different performance from the healthy control group on the neuroticism (p=0.001) and extraversion subscales (p=0.02).

Results from correlation analyses in the tremor-dominant PD group revealed that scores on the BDI-II were associated with performance on attentional matrices (p=0.02) and figure copying test (p=0.02), whereas scores on the SCL-90-R were associated with performance on the immediate recall task on the Auditory Verbal Learning Test (p=0.03). In the akinetic-rigid PD group, results revealed that scores on the BDI-II were associated with performance on the Corsi span forward test (p=0.03), whereas scores on the SCL-90-R were associated with performance on the Corsi span forward test (p=0.02) and Trail-Making Test, part B (p=0.03). Moreover, scores on the EPQ-R neuroticism subscale were associated with performance on the Trail-Making Test, part B (time, p=0.03) and Stroop Color and Word Test (errors, p=0.02), and scores on the EPQ-R extraversion subscale were associated with performance on the MOCA (p=0.02), the immediate recall task on the Auditory Verbal Learning Test (p=0.04), phonological verbal fluency (p=0.03), attentional matrices (p=0.04), the Trail-Making Test, part B (time, p=0.03), and the Stroop Color and Word Test (errors, p=0.03) (Table 4).

Discussion

In the present study, we observed that specific psychological features and personality traits were associated with tremor-dominant and akinetic-rigid phenotypes in the early stage of PD. Indeed, our results from MANOVAs revealed that compared with people with tremor-dominant PD, those with akinetic-rigid PD showed more severe psychological dysfunction, including obsessive-compulsive behaviors with repetitive thoughts and actions, loss of pleasure, pessimism, anxiety, suspiciousness, and isolation. These results are consistent with findings from other studies that observed a strong association between severity of freezing of gait and anxiety (24). In line with this, our results from MANOVAs revealed that people with akinetic-rigid PD showed more severe depression and anxiety, distress from physical problems, negative expectations, self-doubt, feelings of inferiority, irritability, and difficulty in emotion regulation compared with those with tremor-dominant PD and healthy individuals. Therefore, our findings suggest an association between motor symptoms in early-stage PD, such as rigidity and bradykinesia, and more severe psychological dysfunction.

It has been suggested that people with PD show a personality profile characterized by marked neuroticism and low extraversion, with a high tendency to avoid adverse situations (7–13). Our results confirmed that people with early-stage PD, compared with healthy adults, showed an increased tendency to emotional reactivity and a low tendency to interact with other people. Interestingly, we observed that this personality pattern was significantly more severe among people with the akinetic-rigid phenotype of PD than among those with the tremor-dominant phenotype. Indeed, results from MANOVAs revealed that people with akinetic-rigid PD achieved scores on the EPQ-R that were significantly higher on the neuroticism and introversion subscales, compared with those with tremor-dominant PD. Moreover, results from the correlation analyses also confirmed that neuroticism and extraversion personality traits were associated with frontal-executive dysfunction in those with akinetic-rigid PD. Therefore, these results suggest that persons affected by rigid motor manifestations of the disease are particularly vulnerable and sensitive to emotional stimuli, thus producing a higher level of apprehensiveness and a more frequent tendency to avoid social interactions with other people and to prefer social isolation. In line with this, some investigators have observed that people with PD and postural instability and gait difficulty were less extraverted and more neurotic than those with the tremor-dominant form of PD (21, 22). Our results also suggest that psychological alterations, personality traits, and cognitive function are not independent of each other among people with PD. Previous studies that assessed personality traits and cognitive function among patients with PD did not explore this association in subgroups manifesting specific clinical phenotypes of the disease (13, 20, 21). When we examined the possible association of personality traits and cognitive function, we observed in the akinetic-rigid PD group a strong correlation between scores on the EPQ-R neuroticism subscale and performance on the Trail-Making Test, part B, and Stroop Color and Word Test, whereas scores on the EPQ-R extraversion subscale were significantly correlated with performance on the MOCA, Auditory Verbal Learning Test, phonological verbal fluency, attentional matrices, Trail-Making Test, part B, and Stroop Color and Word Test. These relationships suggest that among people with PD and motor symptoms, such as rigidity, the tendency to avoid interactions with other persons and to prefer social isolation is associated with frontal-executive dysfunction, especially in the ability to select and focus attention on relevant features and to inhibit inadequate responses in an effort to engage in relevant behaviors. Therefore, our results confirm previous findings of a prevalent involvement of frontal-executive function in the modification of personality traits among these patients (13, 20, 21). However, we further elucidated that this association was particularly evident among people with nontremor clinical manifestations of PD. Attention to relevant information and activation of inhibitory control mechanisms seem to be crucial factors in interpersonal experiences and emotional and social involvement. Accordingly, frontal-executive dysfunction, particularly in attentional and behavioral control systems, has been previously reported among people with PD (39, 40). Thus, the present findings suggest that common neuroanatomical mechanisms may be involved in the regulation of movement, frontal cognition, and personality processes among people with PD. These mechanisms may involve neurotransmitter pathways in the basal ganglia circuits, and therefore their disruption would result in the different clinical manifestations of the disease, making quality of life worse for people with PD.

There are several limitations to the present study that must be considered. First, we examined a small sample of people with PD who were characterized by a low level of formal education, and this may limit the generalization of our findings. Second, our sample size was relatively small, and because a lower subjects-to-variables ratio results in lower generalizability, our results should be confirmed in studies that include larger samples. Moreover, we mainly assessed frontal-executive function, and therefore investigators in future studies should consider carrying out a wider assessment of other cognitive domains. In addition to the above limitations, we did not evaluate premorbid personality traits, whether people currently living with PD differ from those with a higher risk of future PD in terms of personality, or how having the disease itself and the reaction to having it affects psychological factors. Thus, investigators of future studies should consider these issues and explore the complex interaction between psychological and personality features in these populations.

Conclusions

The findings from the present study provide evidence for a strong association between neuroticism, introversion, and frontal-executive dysfunction in the early manifestation of the akinetic-rigid form of PD. These results support the idea of common mechanisms underlying psychological and motor features, thus contributing to efforts to better refine the clinical manifestation of specific clinical forms of PD. A more comprehensive understanding of the pathogenesis will help clinicians predict these symptoms and develop more targeted treatments that combine pharmacological and psychological strategies to improve the daily lives of people with PD that are associated with emotional and interpersonal dysfunction.