ABSTRACT
Background
Little is known about the cognitive and neuropsychiatric profile associated with punding and hobbyism in Parkinson's disease (PD).
Objective
To compare the clinical and neuropsychological features of PD patients with punding and hobbyism to PD controls.
Methods
The Questionnaire for Impulsive‐Compulsive Disorders in Parkinson's Disease‐Rating Scale (QUIP‐RS) was used as a screening tool, and a structured interview was used to diagnose punding/hobbyism. Clinical and neuropsychological assessment was conducted with validated questionnaires/scales.
Results
Twenty‐one patients with PD and punding (PD + pu) were compared to 26 with hobbyism (PD + h) and 25 PD controls. PD + pu patients showed higher levels of anxiety, non‐motor symptoms and motor symptoms, and lower Frontal Assessment Battery scores. The PD + h group exhibited similar levels of anxiety and motor fluctuations to the PD + pu group.
Conclusion
PD + pu showed increased anxiety and frontal lobe dysfunction, similar to PD + h. Hobbyism could be a prodromal phase with increased risk of leading to punding.
Keywords: Punding, hobbyism, Parkinson's disease, cognitive features, neuropsychiatric features
Punding is a stereotyped non‐goal orientated behavior, characterized by repetitive manipulations of technical equipment, the continual handling, examining, and sorting of common objects, grooming, hoarding, pointless driving, or aimless walkabouts. 1 Initially described among amphetamine and cocaine users, punding was first reported in a levodopa (l‐dopa) treated patient with Parkinson's disease (PD) by Friedman in 1994. 2 The prevalence of reported punding in PD varies between 1.4% 3 up to 14%. 4 Although enjoying a hobby is a healthy habit, when there is frequent preoccupation in pursuing the activity resulting in negative consequences to an individual's personal life it can represent excessive hobbyism, a form of behavioral addiction.
There is an idiosyncratic quality to punding, with previous occupations and pre‐morbid hobbies and pastimes influencing the type of abnormal behavior. 3 Patients with punding have more psychiatric symptoms, greater impulsivity, and are more likely to have other impulsive compulsive behaviors (ICBs). 4 Punding has also been linked with the dopamine dysregulation syndrome 3 (Lees syndrome) 5 and l‐dopa peak dose dyskinesias. 6 Although excessive hobbyism is commonly associated with punding and placed together with punding in the Questionnaire for Impulsive‐Compulsive Disorders in Parkinson's Disease‐Rating Scale (QUIP‐RS), the relationship between these two behavioral abnormalities has not been fully elucidated yet. Hobbyism and punding could represent a spectrum of the same behavior. In this study, we compared the clinical and neuropsychiatric features of PD patients with punding and excessive hobbyism to PD patients without punding and other ICBs.
Methods
PD patients without punding or other ICBs were recruited from a movement disorders outpatient clinic at the National Hospital for Neurology and Neurosurgery, Queen Square, London, United Kingdom (UK).
A diagnosis of punding or hobbyism was made based on the QUIP‐RS using previously published cut‐off scores 7 and confirmed with a structured interview. PD controls also completed the QUIP‐RS and structured interview to confirm the absence of punding or other ICBs. The main features elucidated on interview to distinguish between punding and hobbyism relates to whether the behavior causes occupational and/or social dysfunction (punding) or not (hobbyism), as determined by the treating clinician, following review with the patient, and their carers. Participants self‐completed the following questionnaires: the Hospital Anxiety and Depression Scale (HADS), the 36‐Item Short Form Survey (SF36), the Barratt Impulsiveness Scale (BIS11), the REM Sleep Behavior Disorder Screening Questionnaire (RBDq) and the Apathy Scale (AS). A Unified Parkinson's Disease Rating Scale (UPDRS) parts I and III, the Abnormal Involuntary Movement Scale (AIMS), the Frontal Assessment Battery (FAB), the Montreal Cognitive Assessment (MoCA), and the Stroop test (EncephalApp Stroop Test) 8 were completed by the investigating physician.
The study received approval by the local ethics committee and all participants gave informed consent. All variables were tested for normality and statistical tests were chosen accordingly. Proportions were compared with the Pearson χ2 test, provided the minimum expected cell count was more than five. Data was analyzed using SPSS 22.
Results
Forty‐seven patients screened positive for punding/hobbyism in the QUIP‐RS: 21 were diagnosed with punding as the dominant behavioral phenotype (PD + pu) and 26 with excessive hobbyism without pathological punding (PD + h) after the structured interview. Twenty‐five PD control patients without hobbyism, punding, or other ICBs were matched for age, duration of illness, and medication use (Table 1).
TABLE 1.
Demographic and clinical characteristics
| No. | Punding | Hobbyism | PD controls | |
|---|---|---|---|---|
| 21 | 26 | 25 | Test statistic | |
| Males (%) | 15 (71.4) | 23 (88.5) | 18 (72) | x2 (2) = 2.690; P = 0.261 |
| Age (y) | 59.5 (±16) | 56.0 (±11.7) | 59.8 (±9) | H (2) = 6.549; P = 0.055 |
| Age at PD onset (y) | 47.6 (±9.7) | 42.3 (±10.6) | 47.56 (±7.9) | F (2) = 0.728; P = 0.486 |
| Disease duration (y) | 15.2 (±6.8) | 13.8 (±9.7) | 12.4 (±6.7) | H (2) = 1.832; P = 0.400 |
| Dyskinesias (%) | 16 (80) | 21 (80.8) | 15 (60) | x2 (2) = 3.454; P = 0.178 |
| Motor fluctuations (%) | 20 (95.2) | 23 (88.4) | 18 (72) | x2 (2) = 5.201; P = 0.074 |
| DBS (%) | 4 (19) | 1 (3.8) | 4 (16) | x2 (2) = 2.883; P = 0.237 |
| DA (%) | 9 (42.9) | 13 (50) | 13 (52) | x2 (2) = 0.413; P = 0.813 |
| Amantadine use (%) | 15 (71.4) | 15 (57.7) | 12 (48) | x2 (2) = 2.584; P = 0.275 |
| MAOI use (%) | 6 (28.6) | 3 (11.5) | 3 (12) | x2 (2) = 3.027; P = 0.220 |
| LEDD 9 | 1092 (±333) | 1089 (±495) | 893.8 (±526) | F (2) = 1.457; P = 0.240 |
| DA dose in LEDD | 227 (±165) N = 9 | 175 (±138) N = 13 | 257 (±127) N = 13 | H (2) = 2.916; P = 0.233 |
| HADS | ||||
| Total | 18.2 (±6) | 16 (±5.8) | 13.1 (±6) | F (2) = 3.727; P = 0.029 a |
| Anxiety | 10.4 (±3.9) | 8.5 (±3.7) | 6.8 (±4) | F (2) = 4.631; P = 0.013 a |
| Depression | 7.8 (±3.9) | 7.5 (±3.3) | 6.6 (±3) | F (2) = 0.642; P = 0.529 |
| UPDRS part I | 21.6 (±9.9) N = 20 | 17.7 (±7.4) N = 24 | 13.2 (±5) N = 18 | F (2) = 5.433; P = 0.007 a |
| UPDRS part III | 34.4 (±12.9) | 24.6 (±8.1) | 24.4 (±14) | F (2) = 5.184; P = 0.008 a |
| BIS11 | 67.8 (±8) N = 17 | 67.8 (±6) N = 25 | 64.1 (±6) N = 22 | F (2) = 1.990; P = 0.145 |
| AIMS | 7.7 (±7) | 7 (±5) | 4.8 (±6) | H (2) = 3.282; P = 0.194 |
| FAB | 14.7 (±3) | 16.3 (±1) | 16.6 (±2) | H (2) = 7.634; P = 0.022 a |
| MoCA | 24.3 (±6) | 26.8 (±3) | 27.1 (±2) | H (2) = 2.406; P = 0.300 |
| AS | 15 (±5) N = 18 | 14 (±7) N = 22 | 13 (±5) N = 18 | H (2) = 1.399; P = 0.497 |
| Stroop reaction time (s) | 20.8 (±7) N = 6 | 18.5 (±4) N = 15 | 16.34 (±2.3) N = 12 | F (2) = 2.185; P = 0.130 |
| Stroop errors | 1.4 (±2.5) | 1.25 (±1.5) | 0.42 (±0.5) | H (2) = 1.069; P = 0.497 |
| SF36 general health | 39.9 (±24) N = 20 | 40.9 (±18) | 33.2 (±16) | H (2) = 1.665; P = 0.435 |
PD + pu, patients with Parkinson's disease and punding; PD‐pu, patients with Parkinson's disease without punding; PD, Parkinson's disease; DBS, deep brain stimulation; DA, dopamine agonists; MAOI, monoamine oxidase inhibitors; LEDD, levodopa equivalent daily dose; HADS, Hospital Anxiety and Depression Scale; UPDRS, Unified Parkinson's Disease Rating Scale; BIS11, Barratt Impulsiveness Scale; AIMS, Abnormal Involuntary Movement Scale; FAB, Frontal Assessment Battery; MoCA, Montreal Cognitive Assessment; RBD, REM Sleep Behavior Disorder; AS, Apathy Scale.
Significant results.
Table 1 shows the neuropsychiatric and cognitive characteristics of the three groups. Differences were seen in the HADS anxiety subscale and total score, UPDRS parts I and III, and FAB scores. None of the SF36 subscales differed between PD + pu, PD + h, and controls. Patients with punding showed lower (worse) FAB scores, whereas the MoCA scores difference did not reach significance.
Pairwise post hoc comparisons showed that, compared to controls, individuals with punding exhibited higher scores on the HADS total score and anxiety subscale, higher scores on the UPDRS parts I and III and lower (worse) scores on the FAB. The only difference seen in the comparison between PD + pu and PD + h was a higher burden of motor symptoms and non‐significant lower FAB scores among individuals with punding (see Tables S1 and S2). Among patients with excessive hobbyism: 16 out of 26 had comorbid ICBs (61.5%). Among patients with punding: 12 out of 21 had comorbid ICBs (57%).
Discussion
Punding was associated with increased anxiety, motor and non‐motor symptoms, and frontal lobe abnormalities on neuropsychological testing. The higher anxiety scores are consistent with one previous study in PD patients with ICBs, 9 and, in line with another study, the depression scores did not differ between groups. 10 There is a complex interplay between dopamine and other neurotransmitters that modulate the appearance of anxiety‐like behavior, however the excessive stimulation of dopaminergic D1/D2 receptors of the mesolimbic, mesocortical, and nigrostriatal systems could be driving the increased anxiety seen in the PD + pu group. 11
Most of the patients in this study were male and developed PD at an earlier age, in line with the literature, 12 compatible with our findings. There were no differences in the quality of life between groups, contradicting previous data. 13 Considering that the SF36 is a self‐assessment questionnaire it is possible that patients with punding failed to report difficulties because of lack of insight. In most cases with punding, the patients' carers are more aware than the patient of the negative impact their excessive behaviors are having on their activities of daily living. Another possible explanation is that the SF36 is less sensitive to changes in PD patients as it has been designed as a general quality of life questionnaire.
Supporting existent evidence for frontal lobe dysfunction, patients with punding scored lower than controls on the FAB. This is also consistent with previous studies associating both attentional dysfunction 14 and poorer performance on the Stroop color naming task with thinning of the prefrontal cortex in PD patients with punding. 15 Furthermore, punding also occurs among individuals addicted to cocaine and methamphetamine, 16 conditions that have been associated with frontal dysfunction, 17 and prefrontal cortical thinning on neuroimaging has been described in PD patients with punding. 15 , 18 Considering that the selection of motor programs by the basal ganglia is under prefrontal cortex control through top‐down frontostriatal connections, 19 frontal dysfunction could allow stereotypic behaviors associated with excessive dopaminergic stimulation to evade cortical control.
The pathophysiology of the various types of ICBs appears to differ. Over stimulation of dopaminergic D3 receptors associated with the use of dopamine agonist (DA) are the main risk factors for impulse control disorders, such as hypersexuality, pathological gambling, compulsive shopping and eating. Behaviors that fall on the compulsive spectrum, such as dopamine dysregulation syndrome and punding, have been consistently associated with higher doses of dopaminergic therapy. 3 , 12 Punding behavior is more commonly seen in association with drugs that stimulate dopaminergic D1 and D2 receptors, 10 such as l‐dopa. It is not clear whether the use of DA influences the development of punding, with different groups publishing contradictory findings. 4 , 6 We did not find higher doses of DA in the PD + pu group, suggesting that dopaminergic D3 receptor stimulation associated with the use of DA is not the main mechanism underlying punding.
A higher burden of motor and non‐motor symptoms in patients with punding is reported, which could represent higher PD severity. Because PD pathology affects first, the dorsal striatum, dopaminergic therapy could lead to ICBs by excessive stimulation of the relatively preserved ventral striatum, as suggested in a postmortem study. 20 It is beyond the scope of this paper to assess Lewy body pathology, but theoretically, higher levels of dorsal striatum degeneration could motivate higher intake of PD medication by patients that could, in turn, lead to punding behavior by excessive dopaminergic stimulation of the more preserved mesolimbic pathway. The appearance of punding behavior in animals with preserved nigrostriatal systems and in humans without PD following exposure to drugs of abuse 10 favors this hypothesis. Contradictory findings on the burden of PD symptoms in punding has been published, 21 , 22 and this finding needs to be replicated by future studies.
Patients with excessive hobbyism without pathological punding showed a similar clinical and neuropsychological profile to patients with punding. It is likely that excessive hobbyism in PD is a prodromal phase of punding, and patients with this behavioral abnormality should be watched closely for the development of pathological punding. Furthermore, some of the PD + h exhibit definite ICBs, supporting the idea that individuals with excessive hobbyism could be on their way to developing more serious punding behavior and/or other impulsive compulsive behaviors.
Our sample size is relatively small. This is because we used stringent criteria and only included PD patients who had either no evidence of punding or any other ICBs or had punding or hobbyism as the dominant phenotype. Another limitation is the presence of comorbid ICBs in patients with punding and hobbyism, which could have affected our findings. Nonetheless, this is one of the largest studies looking into cognitive and neuropsychiatric features of punding and excessive hobbyism in PD.
We have found increased anxiety and impaired frontal function in patients with punding. A similar clinical and neuropsychological profile was seen in patients with excessive hobbyism without pathological punding, suggesting that this population is at higher risk of developing punding. Higher stimulation of striatal dopaminergic D1/D2 receptors in individuals with reduced frontostriatal inhibition could be the mechanism behind punding behavior.
Author Roles
(1) Research project: A. Conception, B. Organization, C. Execution; (2) Statistical Analysis: A. Design, B. Execution, C. Review and Critique; (3) Manuscript: A. Writing of the First Draft, B. Review and Critique.
P.B.: 1A, 1B, 1C, 2A, 2B, 3A
S.S.O.S.: 2B, 2C, 3B
E.J.: 2C, 3B
A.J.L.: 2C, 3B
T.T.W.: 2B, 2C, 3B
A.D.: 1A, 1B, 2A, 2B, 2C, 3B
Disclosures
Ethical Compliance Statement
This study was approved by the Queen Square Ethics Committee (reference number 15.LO.1531). Informed consent was obtained from all participants. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this work is consistent with those guidelines.
Funding Sources and Conflicts of Interest
This article presents independent research supported by the Leonard Wolfson Experimental Neurology Centre (LWENC) Clinical Research Facility at the University College London (UCL) Institute of Neurology and UCLH‐National Hospital for Neurology and Neurosurgery, London, UK. We thank the Reta Lila Weston Institute of Neurological Studies for the support received during this research project. P.B.is supported by a grant from Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (Brazilian National Council for Scientific and Technological Development).
Financial Disclosures for the Previous 12 Months
P.B. has nothing to disclose; S.S.O.S has undertaken advisory board work for Novartis and Axis Consultancy; E.J. has nothing to disclose; A.J.L. is funded by the Reta Lila Weston Institute of Neurological Studies, University College London, Institute of Neurology and reports consultancies from Britannia Pharmaceuticals and BIAL Portela, he also reports grants and/or research support from the Frances and Renee Hock Fund, and honoraria from Britannia Pharmaceuticals and BIAL; T.T.W. has received grants from the Medical Research Council, the Reta Lila Weston Trust, Corticobasal Degeneration Solutions, UCLH BRC, The Association of British Neurologists and Rose Trees; and A.D. has nothing to disclose.
Supporting information
Appendix S1. Supplementary Data.
Table S1. Post hoc comparison between patients with punding and controls.
Table S2. Post hoc comparison between patients with punding and hobbyism.
Relevant disclosures and conflicts of interest are listed at the end of this article.
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Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Appendix S1. Supplementary Data.
Table S1. Post hoc comparison between patients with punding and controls.
Table S2. Post hoc comparison between patients with punding and hobbyism.