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Parkinsonism Relat Disord. 2013 November ; 19(11): . doi:10.1016/j.parkreldis.2013.06.018.

Sleep and Impulsivity in Parkinson’s Disease

Michael K. Scullin, Ph.D., Ann B. Sollinger, Ph.D., Julia Land, Psy.D., Cathy Wood-Siverio,
M.S., Lavezza Zanders, B.S., Raven Lee, B.S., Alan Freeman, M.D., Felicia C. Goldstein,
Ph.D., Donald L. Bliwise, Ph.D., and Stewart A. Factor, D.O.*
Department of Neurology, Emory University School of Medicine, Atlanta, GA, USA

Abstract
Background—Impulsive behavior and poor sleep are important non-motor features of
Parkinson’s disease (PD) that negatively impact the quality of life of patients and their families.
Previous research suggests a higher level of sleep complaints in PD patients who demonstrate
impulsive behaviors, but the nature of the sleep disturbances has yet to be comprehensively tested.
Methods—Consecutive idiopathic PD patients (N=143) completed the Minnesota Impulse
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Disorder Interview and a sleep questionnaire that assessed sleep efficiency, excessive daytime
sleepiness, restless legs symptoms, snoring, dreams/nightmares, and nocturia. Patients were also
given a Unified Parkinson’s Disease Rating Scale motor examination and they completed
cognitive testing.
Results—Impulsive PD patients endorsed more sleep complaints than non-impulsive PD
patients. The group difference was primarily attributable to poor sleep efficiency (e.g., greater
nocturnal awakenings), p < .01, and greater daytime sleepiness, p < .01, in the impulsive PD
patients. Interestingly, restless legs symptoms were also greater in the impulsive PD patients, p < .
05. The results could not be explained by medications or disease severity.
Conclusions—Poor sleep efficiency, restless legs symptoms, and increased daytime sleepiness
are associated with impulsivity in PD. Longitudinal studies are needed to determine whether sleep
disturbances precede impulsivity in PD.

Keywords
Parkinson s disease; sleep; impulse control disorder; excessive daytime sleepiness
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1. Introduction
Motor symptoms (i.e. tremor, rigidity, and slowness) are the defining features of Parkinson’s
disease (PD), however, non-motor symptoms may have a greater impact on patients’ quality
of life [1]. Of particular interest, PD is associated with an increased prevalence of impulse
control disorders (ICDs) [2,3]. ICDs include compulsive shopping, compulsive eating,
pathological gambling, dopamine dysregulation syndrome (impulsive dopaminergic
medication use), and hypersexuality which involves exhibitionism, incestuous behavior, and

*
Correspondence: Stewart A. Factor, DO, Emory University School of Medicine, Department of Neurology, 1841 Clifton Road NE,
Atlanta, GA 30329, Phone: 404-728-6238, [email protected].
Financial Disclosures
DLB is a consultant for Ferring Pharmaceuticals, Vantia Therapeutics, and New England Research Institute. SAF is a consultant for
Chelsea, Merz, Ipsen, and ADAMAS, has received grant support from Teva, Ceregene, Ipsen, Allergan, Medtronics, Michael J. Fox
Foundation, has received royalties from Blackwell-Futura and Demos, and has received honoraria for writing and editing from
UpToDate, Current Neurology and Neuroscience. AF has received honoraria from US World Meds and grant support from Adamas
and Merck.
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even zoophilia [2,4]. Impulsivity can greatly impact the lives of patients and their families;
for example, in one case, a PD patient with pathological gambling lost $100,000 [5].
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Dopaminergic medication therapy—particularly the administration of dopamine receptor

agonists—is associated with an increased risk for ICDs in PD patients by about three times
that of those not treated with agonists [6–8]. With the exception of dopamine dysregulation,
ICDs in PD patients have been hypothesized to also relate to non-pharmacological
etiologies, including individual susceptibilities [5]. Risk of ICD in PD patients is associated
with early age of disease onset, novelty seeking, family history of gambling or alcohol
abuse, psychiatric symptoms (e.g., greater depression, anxiety, and obsessive-compulsive
symptoms), and cognitive impairments [9,10].

A feature of ICDs that has received little attention is associated sleep fragmentation and
daytime sleepiness. Sleep deprivation and fragmentation have been linked causally to a lack
of control over impulsive behavior in healthy adults [11,12], presumably due to sleep-loss-
related impairments in prefrontal cortex top-down inhibitory control [13,14]. Likewise, sleep
fragmentation has been linked to impulsiveness in other clinical populations including
attention-deficit/hyperactivity disorder (ADHD)[15] and restless legs syndrome (RLS)[16].
Three reports are suggestive of a similar relationship in PD. Nirenberg and Waters [17]
reported two cases in which ICD development (compulsive eating) was associated with
development of excessive daytime sleepiness. Pontone et al.[18] observed a nominal, but
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non- significant trend for increased PD patient endorsement of sleep disturbance with ICDs.
O’Sullivan et al.[19] had ninety-two PD patients mail in responses to the PD sleep scale and
observed worse overall sleep scores in impulsive compared to non-impulsive patients.

The above studies [17–19] are suggestive of a relationship between sleep and impulsivity in
PD, but they are limited by being either underpowered or by not assessing specific sleep
related symptoms. Our goal in the present study was to assess whether impulsivity is
associated with sleep disturbances across specific domains: sleep efficiency, daytime
sleepiness, nightmares/dreams, snoring, nocturia, and restless legs symptoms. The study
included a relatively large sample of 143 PD patients who were administered a battery of
validated measures in order to permit firmer conclusions about the presence of any
associations.

2. Method
2.1. Patients
The study was approved by the Emory University Institutional Review Board. All
participating subjects reviewed and signed an IRB approved consent document. Subject
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recruitment started February 9, 2009 and ended September 14, 2010. All subjects were
recruited from the practices of two neurologists (SAF and AF) in the Emory University
movement disorder center. The first 79 participants were also part of an initial cohort of 230
PD patients previously enrolled in a genetics study [20]. The last 73 were not part of that
cohort and were recruited consecutively. All patients were evaluated by movement disorder
neurologists (SAF and AF) and met standard clinical diagnostic criteria for PD (modified
UK brain bank criteria)[21]. Patients were enrolled regardless of age at disease onset, family
history of PD, or treatment status (treated or not, with any combination of antiparkinsonian
medications). Exclusion criteria included late stage dementia where subjects were unable to
complete the visit assessments, history of stroke, findings suggestive of atypical
parkinsonism (extraocular movement abnormalities, pyramidal tract signs, ataxia, early
dementia), past neuroleptic use, and past history of multiple head injuries with loss of
consciousness. One neurologist (SAF) rated patients’ motor symptoms in the “on” state
using the Unified Parkinson’s Disease Rating Scale (UPDRS) [22]. Cognitive status was

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determined using the Mini-Mental State Examination (MMSE) [23]. Of the recruited sample
(N = 152), 143 PD patients responded to both the sleep questionnaire and the Minnesota
Impulse Disorder Interview (MIDI) [24]. Demographic information is provided in Table 1.
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2.2. Assessments
The sleep questions are listed in Table 2 and were drawn from existing studies (e.g., restless
legs epidemiology [25,26]). Patients also completed the Epworth Sleepiness Scale [27], in
which they rated how likely they are to doze or to fall asleep in different situations. The
MIDI [24] is a semistructured interview used to assess the degree of impulsivity relating to
compulsive shopping, hypersexuality, and pathological gambling behaviors.

2.3. Statistical analyses

Presence of impulsivity was determined by a “yes” response to any of the MIDI questions
about impulsive buying, gambling, or sexual behavior. For the sleep questionnaire (Table 2),
after removing “don’t know” responses, we compared sleep complaints between the
impulsive PD group and the non-impulsive PD group by using t-tests (Levene’s test
corrections when necessary). In addition, we summed all “yes” MIDI responses to form a
continuous measure of impulsivity and examined sleep—impulsivity associations using
Spearman’s rho.
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Alpha was set to .05, unless otherwise specified. To protect against increases in Type I error,
we combined responses on sleep questions to form composites of total sleep complaints
(summation of questions 2–6, 9–12; see Table 2), frequency of dreams/nightmares
(summation of questions 9–10), restless legs symptoms (summation of questions 11–12),
and sleep efficiency (derived from questions 1–4, 7–8). For the sleep efficiency composite
we first divided the number of hours sleeping at night (question 1) by the amount of time in
bed (absolute difference between questions 7 and 8) and then standardized these values by
converting them to z-scores using SPSS statistical software (i.e., the sample mean is
subtracted from each individual score and the remainder is divided by the standard
deviation). We also calculated the z-scores for questions 2–4 after transforming them with a
sign reversal so that higher values represented better sleep efficiency (less fragmentation).
The sleep efficiency composite was the average of these four z-score measures.

3. Results
3.1. Levels of impulsivity
One hundred and five PD patients were assigned to the non-impulsive group (MMIDI sum =
0.0) and 38 PD patients were assigned to the impulsive group (MMIDI sum = 2.74, SD = 2.89,
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range = 1–10). Most of these patients showed signs of only impulsive buying (n=21), though
some showed only impulsive gambling (n=9), only hypersexuality (n=3), or some
combination (n=5). The impulsive patients and non-impulsive patients did not differ
significantly on any of the demographic or disease-related variables listed in Table 1.

3.2. Sleep and impulsivity

The sleep complaint results are listed in Table 3. The impulsive PD group reported
significantly more sleep complaints than the non-impulsive PD group, and these sleep
complaints were primarily attributable to poor sleep efficiency (i.e., increased fragmentation
of sleep), excessive daytime sleepiness (higher Epworth scores), and increased incidence of
restless legs symptoms. These significant effects replicated when considering impulsivity as
a continuous variable (Spearman’s rho ranged from .20–.25, all ps < .05). The association

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with sleep efficiency related both to difficulty falling asleep, t(141) = 2.13, p = .035, as well
as to more frequent nocturnal awakenings, t(141) = 2.32, p = .022.
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3.3. Sleep and impulsivity by medication class

The relationship between sleep variables and impulsivity was similar when medication class
was considered. When examining PD patients only taking levodopa (n = 33) there was a
significant difference between the impulsive and non-impulsive groups for total sleep
complaints, t(31)=3.67, p<.001, Epworth scores, t(31)=4.01, p<.001, and restless legs
symptoms, t(31)=3.91, p<.001 (a trend was observed for sleep efficiency, t(30)=1.79, p=.
08). Likewise, when examining PD patients only taking dopamine agonists (no levodopa;
n=28), the impulsive group relative to the non-impulsive group demonstrated significantly
more total sleep complaints, t(26)=2.66, p=.013, and greater restless legs symptoms,
t(25)=2.60, p=.015 (Epworth scores and sleep efficiency scores were in the expected
direction and of a similar magnitude but not statistically significant, ps > .10).

3.4. Sleep and impulsivity regression analyses

To rule out the impact of potential covariates we conducted a hierarchical linear regression
on the continuous impulsiveness score. After co-varying for UPDRS, usage of any
dopaminergic medication, MMSE, disease duration, age, years of education, and gender, we
entered in step 2 the total sleep complaints score, which explained significant additional
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variance in impulsiveness, ΔR2 = .062, β = .258, p = .003. In a second hierarchical

regression analysis, we replaced the total sleep complaints score with the sleep efficiency
composite, restless legs symptoms, and Epworth scores (in step 2). These three measures
collectively explained significant variance in impulsiveness, ΔR2 = .076, p = .018; of these
three measures, only sleep efficiency explained significant unique variance, β = −.226, p = .
014. We more closely examined the sleep efficiency effect by entering in step 2 the reported
difficulty falling asleep and frequency of nocturnal awakenings. These two measures
combined to explain significant variance in impulsiveness, ΔR2 = .065, p = .010, and
nocturnal awakenings was a stronger contributor, β = .215, p = .018, than difficulty falling
asleep, β = .113, p = .196.

4. Discussion
Sleep disruption has been linked causally to a lack of control over impulsive behavior in
healthy individuals [11,12], and is associated with impulsivity in some neurologic disorders
[15,16]. Previous research has provided suggestive data that impulsivity in PD patients is
also associated with sleepiness and sleep disturbances [17–19]. The present findings confirm
that impulsivity in PD is linked to sleep features, particularly excessive daytime sleepiness
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(Epworth scores) and sleep fragmentation (i.e., poor sleep efficiency). Disease-specific
factors and/or individual susceptibility may explain these findings [5].

4.1. Disease and medication-specific factors

Impulsivity in PD first received attention over a decade ago due to its association with
dopaminergic medication [2,7]. Impulsivity is linked more to dopamine agonists than
levodopa [6], and may or may not be related to dosage [5,8]. In addition, greater daytime
sleepiness has been linked to dopaminergic medications (particularly dopamine agonists),
but such effects are not strongly related to nocturnal sleep [28]. In the present study,
regression analyses demonstrated associations between sleep and impulsivity after
controlling for usage of dopaminergic medication; the sleep—impulsivity link was also
observed when isolating both levodopa and dopamine agonist drug classes.

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A limitation of the present study was a lack of information on medication doses, therapy
duration, and reliance on “on” state exams. Though limiting, available measures of disease
progression did not explain the sleep—impulsivity association. There were no significant
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differences between the impulsive and non-impulsive PD groups in disease severity as

measured by UPDRS motor score in the “on” state, disease duration, or cognitive ability
(MMSE). Therefore, though dopamine dysregulation plays an important role in increasing
risk of impulsivity in PD, it is not the only important variable [5], and the sleep—
impulsivity relationship appears to go beyond medication effects.

4.2. Individual susceptibility

Another explanation of the sleep—impulsivity association in PD patients is that nocturnal
sleep disturbances and daytime sleepiness increase susceptibility to developing an ICD.
Sleep deprivation and sleepiness are known to increase impulsive behavior [11,12], either
via disruption of the prefrontal cortex [13,14], which would otherwise provide top-down
inhibitory control of impulsive behavior, or by amplifying the reactivity of brain reward
networks [29]. Moreover, PD is associated with impairments to sleep including sleep
fragmentation [30]. Case reports have suggested an association in PD patients between
impulsivity and increased daytime sleepiness [17], and PD patients with impulsivity
generally endorse more sleep complaints [18,19]. We confirmed and elucidated the nature of
these associations with the Epworth sleepiness scale and a composite measure of sleep
efficiency. It may be important to note that these effects occurred in the absence of a
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significant difference in total sleep time between impulsive and non-impulsive groups.
Group differences in sleep fragmentation (and restless legs) are possible in the absence of
differences in total sleep time (see Sleep Heart Health Study [31]). However, this null effect
may have been due to insufficient statistical power (the groups differed by approximately 23
minutes) or participant confusion over the difference between total sleep time and total time
in bed. We observed that sleep efficiency was the most potent of the sleep variables in
explaining variance in impulsiveness, and the sleep efficiency effect was due more to
frequency of nocturnal awakenings than to difficulty falling asleep. The latter pattern is
more consistent with the idea of sleep deficiencies contributing to risk for ICDs than the
hypothesis that ICDs cause difficulties with falling asleep at night. However, longitudinal
studies that include caregiver reports are needed to determine whether sleep disturbances
precede impulsive behaviors in PD patients.

4.3. PD, impulsivity, and restless legs

A final, unexpected result was that we observed an association between restless legs
symptoms and impulsiveness in PD patients, which has not been previously reported.
Though speculative, it is possible that the urge to move ones legs and the urge to
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compulsively gamble, shop, or have sex, constitutes a shared phenomenology of restless legs
and PD plus impulsivity. The increased prevalence of restless legs symptoms in PD patients
with impulsiveness warrants further attention.

4.4. Conclusions
We observed an association in PD patients between impulsivity and sleep disturbances
including frequency of nocturnal awakenings, difficulty falling asleep, restless legs
symptoms, and excessive daytime sleepiness. The association between impulsivity and sleep
disturbances could not be attributed solely to disease- or medication-related factors.
Longitudinal studies that investigate time of onset of sleep disturbances and impulsive
behaviors will help determine whether impulsive behaviors cause nocturnal sleep
disturbances or if sleepiness and disturbed nocturnal sleep increase vulnerability to
developing ICDs.

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Acknowledgments
This work was supported by the Consolidated Anti-Aging Foundation, The Sartain Lanier Family Foundation, Inc,
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and the National Institutes on Health (grant number R01 NS-050595 to D.L.B., and F32 AG-041543 to M.K.S.).
M.K.S. was partially supported by an Emory University School of Medicine Cottrell Fellowship.

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Table 1
Demographic information (standard deviations in parentheses) across the non-impulsive PD group and
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impulsive PD group. UPDRS (n=142), MMSE (n=141), and medication class (n=142) information was
available for most patients. P values refers to the independent samples t test between the non-impulsive and
impulsive PD groups.

PD Total Non-Impulsive PD Impulsive PD P

Group Group Group value
(n=143) (n=105) (n=38)
UPDRS Motor 17.77(7.88) 17.46(7.81) 18.63 (8.11) .44
Scale

MMSE (max=30 28.21 (1.96) 28.29 (1.91) 27.97 (2.09) .35

points)

Disease Duration 7.95(4.40) 7.87 (4.12) 8.18 (5.17) .71

(years)

Age (years) 64.71(9.05) 64.50 (9.17) 65.26 (8.82) .66

Education (years) 15.76(2.31) 15.76 (2.21) 15.76 (2.63) .99

Gender (% Female) 35 32 42 .28

Levodopa (% on 52 49 62 .15
med)
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Dopamine agonist 49 48 51 .69

(% on med)

PD=Parkinson’s disease; UPDRS=Unified Parkinson’s Disease Rating Scale; MMSE=Mini-Mental State Examination
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Table 2
Sleep questionnaire, scale of individual sleep questions, and composite score subdivisions.
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Sleep Question Scale Composite

1. How many hours do you usually get at Sleep efficiency
night?

2. How often do you have trouble falling 1 to 5 Sleep efficiency

asleep?

3. How often do you have trouble waking up 1 to 5 Sleep efficiency

during the night?

4. How often do you have trouble waking up 1 to 5 Sleep efficiency

too early and not being able to fall asleep again?

5. When you awaken during the night, how 1 to 4 Nocturia

often do you urinate?

6. How often do you snore in any way? 1 to 5 Snoring

7. What time do you typically go to bed at Sleep efficiency

night?

8. What time do you typically wake up in the Sleep efficiency

morning?

9. How often do you have a night full of 1 to 5 Dreams/Nightmares

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intense, vivid dreams?

10. How often do you have nightmares 1 to 5 Dreams/Nightmares

(frightening dreams)?

11. At bedtime, how often does restlessness in 1 to 4 Restless Legs

your legs delay your falling asleep?

12. When you wake up during the night, how 1 to 4 Restless Legs
often do you feel unpleasant sensations in the
leg muscles that require you to move your legs
or walk in order to be comfortable?

Questions 2–4, 6, 9–10: 1 = never, 2=A few times, 3=Sometimes, 4=Quite often, 5=Usually, 6=Don’t know. Question 5: 1=Once, 2=Twice,
3=Three Times, 4=Four or more times. Questions 11–12: 1=Never, 2=Occasionally, 3=Often, 4=Very often
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Table 3
Sleep questionnaire responses across non-impulsive and impulsive PD groups. Standard deviations are in
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parentheses.

Non-Impulsive Impulsive PD p value

PD Group (n=105) Group (n=38)
Total Sleep Complaints Score 17.19 (4.06) 19.95 (4.96) <.001***

Sleep Efficiency Z-Composite .10 (.64) −.26 (.77) .008**

Restless Legs 2.96 (1.26) 3.55 (1.52) .021*

Dreams/Nightmares† 3.23 (1.30) 3.83 (1.70) .057

Nocturnal Sleeping Hours 6.96 (1.29) 6.58 (1.36) .138

Bathroom trips 1.63 (.81) 1.92 (1.00) .083

Snoring 2.75 (1.15) 3.06 (1.29) .205

Epworth Score 9.00 (4.50) 11.58 (5.24) .005**

Note:
†
indicates that Levene’s test for equality of variances was significant (p < .05) and the adjusted p value is reported. The sample sizes varied due to
missing data or “don’t know” responses. The available sample sizes were 137 for sleep efficiency, 141 for restless legs, 137 for dreams/nightmares,
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140 for nocturnal sleeping hours, 142 for nocturia, 125 for snoring, and 141 for Epworth. PD=Parkinson’s disease
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