Journal of the International Neuropsychological Society (2011), 17, 841–852.
Copyright E INS. Published by Cambridge University Press, 2011.
Relation of Parkinson’s Disease Subtypes to Visual
Activities of Daily Living
Daniel R. Seichepine,1Sandy Neargarder,1,2Ivy N. Miller,1Tatiana M. Riedel,3Grover C. Gilmore,3AND
1Department of Psychology, Boston University, Boston, Massachusetts
2Department of Psychology, Bridgewater State University, Bridgewater, Massachusetts
3Mandel School of Applied Social Sciences, Case Western Reserve University, Cleveland, Ohio
(RECEIVED August 19, 2010; FINAL REVISION May 25, 2011; ACCEPTED May 25, 2011)
Visual perceptual problems are common in Parkinson’s disease (PD) and often affect activities of daily living (ADLs).
PD patients with non-tremor symptoms at disease onset (i.e., rigidity, bradykinesia, gait disturbance or postural
instability) have more diffuse neurobiological abnormalities and report worse non-motor symptoms and functional
changes than patients whose initial symptom is tremor, but the relation of motor symptom subtype to perceptual deficits
remains unstudied. We assessed visual ADLs with the Visual Activities Questionnaire in 25 non-demented patients with
PD, 13 with tremor as the initial symptom and 12 with an initial symptom other than tremor, as well as in 23 healthy
control participants (NC). As expected, the non-tremor patients, but not the tremor patients, reported more impairment
in visual ADLs than the NC group, including in light/dark adaptation, acuity/spatial vision, depth perception, peripheral
vision and visual processing speed. Non-tremor patients were significantly worse than tremor patients overall and on light/
dark adaptation and depth perception. Environmental enhancements especially targeted to patients with the non-tremor PD
subtype may help to ameliorate their functional disability. (JINS, 2011, 17, 841–852)
Keywords: Parkinsonism, Tremor, PD subtype, Activities of daily living, Neuropsychology, Quality of life
Parkinson’s disease (PD) has traditionally been viewed as a
movement disorder characterized by resting tremor, rigidity,
of the disease are also experienced by the majority of patients
(,83%; Shulman, Taback, Bean, & Weiner, 2001) including
disorders of sensation and perception, mood, sleep, and cog-
nition (for recent reviews, see Chaudhuri & Schapira, 2009;
Cronin-Golomb, 2010; Pandya, Kubu, & Giroux, 2008;
Poewe, 2008). These non-motor symptoms are as debilitating
as the motorsymptoms andmayactuallybe better predictors of
quality of life (Witjas et al., 2002). Patients with worse non-
motor symptoms report more impairments in overall daily
functioning (Hariz & Forsgren, 2011). Objective measures of
non-motor symptoms, such as visual testing, have been found
to relate to performance on certain activities of daily living
(ADL), such as driving a car (Amick, Grace, & Ott, 2007;
Uc, Rizzo, Johnson, et al., 2009). Visual perceptual deficits
are of particular relevance to vision-based ADLs.
Patients with PD exhibit an array of visual perceptual
deficits, ranging from problems with basic abilities such as
detecting color (Buttner et al., 1993; Diederich, Raman,
Leurgans,& Goetz, 2002;Lee & Harris, 1999; Price, Feldman,
Adelberg, & Kayne, 1992) and perception of planar motion
and optic flow (Davidsdottir, Wagenaar, Young, & Cronin-
Golomb, 2008) to higher-order abilities such as facial emotion
recognition (Clark, Neargarder, & Cronin-Golomb, 2008) and
facial scanning (Clark, Neargarder, & Cronin-Golomb, 2010).
Numerous studies indicate that patients with PD experience
and Yahr (1978) found that patients with PD displayed greater
latencies to visual evoked potentials than did a control group
in response to sinusoidal contrast gratings, providing initial
evidence for visual perceptual deficits. Reduced contrast sen-
sitivity in PD has since been reported using low-contrast letter
reading charts (e.g., Regan & Neima, 1984; Regan & Maxner,
1987) and computer-based measures (e.g., Amick, Cronin-
Golomb, & Gilmore, 2003; Davidsdottir et al., 2008). These
changesin contrast sensitivity arenot benign as theyhavebeen
Correspondence and reprint requests to: Alice Cronin-Golomb, Department
of Psychology, Boston University, 648 Beacon Street, 2nd floor, Boston, MA
02215. E-mail: email@example.com
related to quality of life in PD. For example, poor contrast
sensitivity is associated with worse driving performance
(Amick et al., 2007; Devos et al., 2007; Uc, Rizzo, Anderson,
et al., 2009; Worringham, Wood, Kerr, & Silburn, 2006) and
with motor freezing and hallucinations (Davidsdottir, Cronin-
Golomb, & Lee, 2005).
In addition to deficits in basic visual functioning, patients
with PD experience problems with higher-level visuospatial
functioning, which may affect performance on ADLs.
Visuospatial functioning includes perceiving the spatial
relations among visual stimuli, a skill necessary to perform-
ing everydaytasks such as preparing meals, driving a car, and
selecting medications. Experimental studies have shown that
several aspects of visuospatial functioning are impaired in
PD, including spatial navigation, mental rotation, hierarchical
pattern perception, facial emotion recognition, spatial working
memory and spatial planning (Altgassen, Phillips, Kopp, &
Kliegel, 2007; Amick, Schendan, Ganis, & Cronin-Golomb,
2006; Clark et al., 2008; Cronin-Golomb, 2010; Davidsdottir
et al., 2008; Kemps, Szmalec, Vandierendonck, & Crevits,
2005; Lee, Harris, & Calvert, 1998; Montse, Pere, Carme,
Francesc, & Eduardo, 2001; Possin, Filoteo, Song, & Salmon,
2008; Schendan, Amick, & Cronin-Golomb, 2009; Siegert,
Weatherall, Taylor, & Abernethy, 2008). These findings are in
line with studies using self-report measures, through which PD
patients report problems judging distances (Davidsdottir et al.,
2005; Lee & Harris, 1999; McDowell & Harris, 1997a). The
relation between these visuospatial changes and performance
on a variety of everyday tasks is less clear. Klepac, Trkulja,
Relja, and Babic ´ (2008) reported that better performance
on neuropsychological tests of visuospatial and executive
functioning were related to better health-related quality of life
as indicated by self report (Parkinson’s Disease Questionnaire;
PDQ-39).Studies using morenaturalisticdesignshave reached
similar conclusions. For example, Uc and colleagues (2007)
examined the relation between driving and neuropsychological
performance. They found that performance on visuospatial and
executive functioning tasks but not on tasks of motor function
predicted driving performance, suggesting that the non-motor
symptoms of PD are at least as detrimental to everyday func-
tioning as the motor symptoms.
including in terms of perceptual abilities, and this heterogeneity
may be related to daily function. Attention is being turned
increasingly to the type of initial symptom of PD (Lewis et al.,
2005) as a major source of heterogeneity, with differences
emerging between patients presenting with resting tremor
versus non-tremor symptoms. The non-tremor subtype is also
referred to as akinetic-rigid or postural instability-gait difficulty
(PIGD; Zaidel, Arkadir, Israel, & Bergman, 2009). Multiple
single-photon emission studies have demonstrated negative
correlations between striatal uptake of dopamine and non-
tremor symptoms (i.e., rigidity, bradykinesia, gait, balance, and
posture) but not tremor symptoms, indicating that these two
types of motor symptoms likely arise from disturbances of dif-
ferent neural systems (Benamer et al., 2000; Bru ¨cke et al. 1997;
Seibyl et al., 1995; Shinotoh, Uchida, Ito, & Harrori, 2000;
by post-mortem studies indicating more diffusely located cor-
tical Lewy bodies (Selikhova, Williams, Kempster, Holton, &
Lees, 2009) and greater dopamine loss within the ventral rostral
region of the globus pallidus in cases with non-tremor onset
progression and more frequent dyskinesias, gait disorders and
falls (Rudzinska et al., 2007). They appear to be more suscep-
tible to non-motor symptoms than the tremor-onset subtype
(Reijnders, Ehrt, Lousberg, Aarsland, & Leentjens, 2009),
including slower psychomotor speed and decreased cognitive
flexibility (Lyros, Messinis, & Papathanasopoulos, 2008), pro-
cedural learning (Vakil & Herichanu-Naaman, 1998), atten-
tional decline (Taylor et al., 2008), more frequent dementia
Rajput, 2009), and more frequent depression (Burn et al., 2003;
Lewis et al., 2005). Additionally, non-tremor onset patients
have reported poorer ADLs than tremor onset patients (Hariz
for self-care that rely on visual functioning) have not yet been
examined for these subtypes of PD.
Previous reports linking visual deficits to impaired func-
tional performance in PD have primarily focused on contrast
sensitivity and on driving competence in PD without reference
to subtypes. The present study expands the scope of investi-
gation by using visual assessments together with a validated
self-report measure (Visual Activities Questionnaire; VAQ)
to identify the extent to which visual ADLs are compromised
by PD and to determine which specific visual domains are
most affected in the tremor and non-tremor PD subtypes. We
hypothesized that the non-tremor onset subtype would report
more problems with visual ADLs, consistent with recent evi-
dence suggesting that this subtype experiences a wide range
of non-motor symptoms, including difficulties with ADLs in
ADL domains affected may point to specific interventions to
improve ADLs and quality of life in PD.
Participants included 25 individuals with PD (12 women,
13 men) and 23 age and education-matched normal control
participants (NC; 11 women, 12 men). The PD participants
were grouped by type of initial motor symptom: tremor
dominant onset (TD; 6 women, 7 men) or non-tremor domi-
nant onset (NTD; 6 women, 6 men). Five of the NTD subtype
participants had initial symptoms starting on the left side
ofthe body and seven had symptomsstarting on the right side
of the body. In the TD subtype, seven participants’ initial
symptoms were on the left side and six on the right side.
Demographic characteristics were similar between partici-
pants with respect to side of initial symptom. Characteristics
D.R. Seichepine et al.
of the TD and NTD subtypes are listed in Table 1. All parti-
cipants provided informed consent for the protocol approved
by the Boston University Charles River Campus Institutional
PD patients were recruited from the Parkinson’s Disease
from the general community. Exclusion criteria included co-
existing serious chronic medical illnesses (including psychiatric
Table 1. Participant characteristics
NC Tremor-onset PD
Non-tremor onset PD
Hoehn & Yahr stage
UPDRS Motor score
UPDRS Rigidity score
UPDRS Bradykinesia score
UPDRS Tremor score
UPDRS Gait score
UPDRS Right-side symptoms
UPDRS Left-side symptoms
Duration of illness (yrs)
Geriatric Depression Scale
Overall mod-MMSE (converted)
Attention and Calculation
Longest Digit Span Forward
Longest Digit Span Backward
Near acuity (log-transformed)
Far acuity (log-transformed)
FACT log contrast sensitivity: near
FACT log contrast sensitivity: far
Note. Values represent means and standard deviations except near and far acuity, which are reported as medians, and Hoehn & Yahr scores,
which are reported in median and range. Hoehn and Yahr stage is an index of motor severity in PD. LPD, RPD: left- and right-onset
Parkinson’s disease. FACT5Functional Acuity Contrast Test. UPDRS5Unified Parkinson’s Disease Rating Scale. cpd5cycles per degree.
*indicates PD group differed from NC (p,.05); **indicates PD group differed from NC (p,.017).
1indicates PD groups differed from each other (p,.05); 11 indicates PD groups differed from each other (p,.017).
Visual ADLs in Parkinson’s disease
or neurological), use of psychoactive medications besides anti-
depressants and anxiolytics in the PD group, use of any psy-
choactive medications in the NC group, history of intracranial
surgery, traumatic brain injury, alcoholism or other drug abuse,
or eye disease or abnormalities as noted on an eye examination.
Seventeen of the 23 NC and 17 of the 25 PD participants
received a detailed neuro-ophthalmological examination to rule
out visual disorders arising from dysfunction of anterior path-
ways,including cataracts, glaucoma, and macular degeneration.
There were no differences between those who completed the
neuro-ophthalmological examination and those who did not on
any of the visual measures or the VAQ. Participants used their
own refractive correction for all testing.
ratio. No participants were demented, with all obtaining scores
of 27 or above on the standard Mini-Mental State Examination
(four NC) or 25 or above on the Modified Mini-Mental State
Examination (all other participants; overall scores converted
to the standard MMSE scale). Because the Modified MMSE
in the absence of dementia, we used a cut-off score of 25 rather
than the standard MMSE cut-off of 27. Mean scores for both
the tremor onset subtype (27.4; SD5.82) and non-tremor onset
subtype (28.0; SD51.5) were worse than for the NC group
Analyses of the Modified MMSE subscales were con-
ducted to examine potential cognitive differences between
groups and post hoc comparisons were corrected to .017 for
the number of groups (.05/3). All groups performed similarly
on orientation (p5.99), registration (all groups performed
without error), recall (p5.12), general knowledge (p5.46),
confrontation naming (p5.67), language (p5.09), and
construction (p5.23) (performance near ceiling in all cases).
The TD group had lower scores on digit span than the NC
group (p,.017); NTD and NC participants received the
maximum subscale score (10 of 10). The digit span subscale
of the Modified MMSE differs from traditional digit span
scores as up to only 10 points can be awarded (up to 6 for
digits forward and up to 4 for digits backward). NTD patients
performed more poorly than NC on attention and concentra-
tion (i.e., serial sevens and adding change; p,.017), and
there was a trend for TD patients to perform more poorly than
NC (p5.03). There was no difference between the two PD
In addition to MMSE, verbal fluency (category-animals
and letter ‘‘F’’) and traditional (longest) digit span forward
and backward were also assessed for the PD participants. The
TD and NTD groups performed similarly on both measures
of verbal fluency and on longest digit span backward, but the
TD group performed more poorly than the NTD group on
longest digit span forward (p,.05).
PD patients endorsed more depressive symptoms on the
Geriatric Depression Scale (GDS; Yesavage et al., 1983)than
the NC (t (46)52.7; p,.01). Patients with the tremor onset
and non-tremor onset subtypes indicated similar levels of
depression (t(23)50.3; p5.77). PD participants had mild to
moderate motor symptoms as indicated by a median stage II
Hoehn and Yahr score (Hoehn & Yahr, 1967) with a stage
range of I to III. Motor scores on the Unified Parkinson’s Dis-
NTD group(t(23)52.2,p,.04),indicatingthat theTD group
had worse overall motor scores. Motor symptom scores for the
rigidity, bradykinesia, gait, and tremor subscales were similar
for the PD subgroups. The mean duration of illness was similar
for NTD (8.6 years) and TD (8.9 years). Overall, the TD group
had more severe motor symptoms (as indicated by UPDRS
total motor score) than the NTD group, despite the groups
being similar in cognitive performance. All participants were
tested while they were in the ‘‘on’’ stage of medication effec-
tiveness. For PD, levodopa equivalent dosages (LED) were
calculated based on previous reports with LED: (regular levo-
dopa dose31)1(levodopa controlled-release does3.75)1
(rotigotine316.67)1(pergolide dose and cabergoline dose3
dose1levodopa controlled-release dose3.75]3.25) if tak-
ing tolcapone or entacapone. Mean LED was 545.4mg
(standard deviation5329.6). Of 21 PD patients who pro-
vided details of their medications, 17 (81%) were on a com-
bination of carbidopa and levodopa and 17 patients (81%)
were also taking a DA agonist including three of the four who
were not on a combination carbidopa/levodopa medication.
Overall, 20 of the 21 participants (95%) were on one or both
of these medications. PD symptoms in the remaining parti-
cipant were being treated with an MAO inhibitor (selegiline).
Five patients were on a COMT inhibitor (mean5575mg;
Measures and Procedures
Participants were administered the VAQ and several mea-
sures of basic visual functioning. Visual functioning was
assessed at both near and far distances because deficits may
occur at one distance and not the other, and these differences
may relate to different types of visual ADLs. For example,
deficits at closer distances may affect reading, whereas
deficits at farther distances may affect driving.
Acuity Snellen eye charts (Lighthouse, Long Island City,
New York) were used to measure binocular visual acuity at
10 feet for far acuity and 16 inches to the corner of the eye for
near acuity. Participants read a series of progressively smaller
letters starting at the top row (largest) and move down until
they can no longer identify one half of the letters on that row.
Standard Snellen scores (minimal angle of resolution) were
log-transformed to perform group comparisons.
Contrast Sensitivity was assessed binocularly with near
(16 inches) and far (10ft) Functional Acuity Contrast Test
Charts (FACT: Stereo Optical, Chicago, IL). The FACT
assesses the degree of contrast at which an individual can
correctly detect the orientation of sinusoidal gratings at various
spatial frequencies. The stimuli are presented in nine rows of
circles that decrease in contrast from left to right. Moving
down each column, the gratings increase in spatial frequency,
D.R. Seichepine et al.
from 1.5, 3, 6, 12, to 18 cycles per degree (cpd). In each
circle, the gratings are oriented either vertically, to the left, or
to the right and the participant indicates the orientation, either
each spatial frequency by finding the minimal perceptible
contrast level required to correctly identify the orientation of
the grating for a given row. Higher scores indicate better
contrast sensitivity. Participants who could not recognize the
highest contrast level for each spatial frequency were excluded
The Visual Activities Questionnaire (Sloane, Ball, Owsley,
effect of vision on performing everyday tasks. Participants are
provided the following instructions printed on the top of
the questionnaire: ‘‘On the next few pages you’ll read some
statements about problems youmay encounterduringactivities
which involve vision. Read each statement carefully. Then
indicate how frequentlyyou havethe problem, by choosingthe
word beneath the statement that best applies to you and your
your glasses or contact lenses (if any).’’ For each statement,
participants place a mark to indicate the frequency at which
problems occur on a five-point scale: never, rarely, sometimes,
often, or always. On the five items that ask about driving a car,
participants can also mark ‘‘do not drive’’ and these scores are
removed from subscale calculations. Higher scores indicate
worse visual functioning. Items load onto one of eight
subscales: color discrimination (three items), glare disability
(three items), light/dark adaptation (four items), acuity/spatial
vision (four items), depth perception (three items), peripheral
vision (five items), visual search (five items), and visual
processing speed (six items). Participants were provided as
much time as required to complete the questionnaire.
Visual Functioning by Group
Acuity scores were similar among the three groups at both
near (F(2,45)50.9; p5.42) and far (F(2,45)51.6; p5.21)
The FACT contrast sensitivity test provides data at specific
cycles per degree (cpd). For near FACT, four PD participants
(three non-tremoronset)couldnotsee eventhehighestcontrast
spatial frequency(18.0cpd) using an independent groupst test.
By analyzing the data separately we avoided the elimination of
the four participants’ data in the frequencies below 18.0 cpd.
Aone-tailedmixeddesignanalysis of variance (ANOVA) with
group serving asthe between group factor (NC, TD, and NTD)
and frequency (1.5, 3.0, 6.0, 12.0 cpd) serving as the within
group factor indicated a significant main effect of spatial
frequency (F(2.2, 95.7)594.8; p,.001), a significant main
effect of group ( F(2,44)56.7; p,.002), and a significant
interaction between group and spatial frequency (F(4.4,
95.753.0; p,.01). Post hoc analyses for the interaction
indicated that the NTD group had reduced contrast sensitivity
relative to NC at 3.0 cpd (p,.02), 6.0 cpd (p,.01), and
12.0 cpd (p,.002), and relative to the TD group at 3.0 cpd
(p,.02) and 12.0 cpd (p,.04). NC and the TD group per-
formed similarly to each other across spatial frequencies. For
the 18.0 cpd condition, there were no significant differences
between groups (F(2,41)51.9; p5.08).
For the far FACT, one NTD and two NC participants could
not see the highest contrast level at 18.0 cpd, and data were,
therefore, analyzed separately as described above. This is
typical of normal aging (reviewed in Owsley, 2010). For the
first four spatial frequencies, we observed a significant main
effect of spatial frequency (F(2.7, 121.4)573.8; p,.001),
and a significant main effect of group (F(2,42)52.8;
p,.04), but no interaction between group and spatial fre-
quency (F(5.4, 121.4)5.60; p5.38). After correcting for
multiple comparisons, post hoc analyses were not significant
for any comparison. For the 18.0 cpd condition, there was a
significant difference between groups (F(2, 42)52.6;
p,.04), however, corrected post hoc analyses did not reveal
any notable differences between the three groups.
Statistical analyses of the VAQ
Non-parametric statistics were used to perform all ana-
lyses. Effects of group (TD, NTD, NC) were examined by
the Kruskall-Wallis test and when indicated (alphar.05),
post hoc analyses were performed (Mann-Whitney U test).
Post hoc analyses were adjusted for multiple comparisons
using Bonferroni’s correction (.05/35.017). Spearman rank
correlation coefficients were used to determine dependence
between variables. Although individuals with PD endorsed
more depressive symptoms on the Geriatric Depression Scale
than did NC, results were not correlated with performance
on any of the VAQ subscales for either group, indicating
that depression differences were not responsible for the
significant group findings.
Scores on the VAQ by group
The Kruskall-Wallis test revealed significant differences by
group (NC, TD, NTD) on the overall composite score
(H(2)58.9; p,.05). Post hoc analyses were adjusted for
multiple comparisons using Bonferroni’s correction and
indicated that the NTD group endorsed more problems than
either the NC group (U562.0; p,.017) or the TD group
(U530.0; p,.017). There was no difference in scores
between NC and the TD group (U5130; p5.54). Medium
to large effect sizes were observed for the NTD group com-
pared to NC (r52.45) and the NTD group compared to TD
group (r52.52) (Figure 1).
Visual ADLs in Parkinson’s disease
Analyses of the eight subscales by group
Kruskall-Wallis tests were performed at each subscale to exam-
ine potential group differences. Significant group differences
were observed on the subscales for light/dark adaptation
depth perception (H(2)59.3; p,.01), peripheral vision
(H(2)59.7; p,.01), and visual processing speed (H(2)57.7;
p,.05). Post hoc analyses were performed and were adjusted
for multiple comparisons using Bonferroni’s correction.
There were no significant differences in scores between the NC
and TD group. The NTD group endorsed more problems than
the NC group on light/dark adaptation (U565.5; p,.017),
acuity/spatial vision (U569.5; p,.017) depth perception
visual processing speed (U566.5; p,.017). When compared
to the TD group, the NTD group endorsed more problems on
light/dark adaptation (U531.0; p,.017) and depth perception
(U533.0; p,.017). Effect size analyses were performed
when appropriate using Pearson’s correlation coefficient.
Medium to large effect sizes were observed for the NTD
group compared to the NC on light/dark adaptation (r52.43),
acuity/spatial vision (r52.40), depth perception (r52.47),
peripheral vision (r52.49), and visual processing speed
depth perception (r52.51). See Figure 2.
Correlations between VAQ scores and vision results
Correlations between vision scores and the VAQ were
determined by Spearman rank correlation coefficients for NC
and for the two PD subgroups. All significant correlations are
shown in Table 2. For analyses, FACT levels were grouped
according to whether they were low (1.5, 3.0 cpd), middle
(6.0, 12.0 cpd), or high spatial frequencies (18.0 cpd). Lower
scores on the FACT indicate worse contrast sensitivity and
ADLs; hence, negative correlations indicate more problems
with visual ADLs with poorer contrast sensitivity. All cor-
relations for the NC group were negative, as expected. No
correlations were significant for the NT group. For the tre-
mor-onset group, correlations with the acuity/spatial vision
subscale were negative; correlations with other subscales
were positive. In light of the number of correlations and the
resulting limitation of statistical power, these comparisons
should be considered exploratory in nature.
We found that PD patients without tremor as the initial
symptom experienced more problems with visual ADLs than
did either PD patients with tremor as the initial symptom or
healthy control adults. This finding is consistent with recent
evidence suggesting that non-tremor onset PD is associated
withawide rangeofnon-motor symptomsandproblems with
ADLs in general. Group differences were observed between
the non-tremor onset patients and the NC group in five of the
eight visual domains tested by the VAQ, including light/dark
adaptation, acuity/spatial vision, depth perception, peripheral
vision, and visual processing speed. PD subtype differences
were also observed, with the non-tremor patients reporting
more problems with light/dark adaptation and depth percep-
tion than the tremor subtype. By contrast, PD partici-
pants with tremor as the initial symptom indicated levels of
functioning similar to the NC group in all visual ADL
domains. This finding accords with reports indicating that
the tremor subtype experiences fewer and less severe non-
motor symptoms of PD than does the non-tremor subtype
Tremor onset PD
Non-tremor onset PD
Frequency of problems
Fig. 1. Mean total score on the VAQ for NC, Tremor onset PD and
Non-tremor onset PD. Error bars represent standard errors of the
mean. The Non-tremor onset PD patients indicated worse function-
ing than the NC (p,.017) and Tremor onset PD groups (p,.017).
CD GD LDA ASV DPPV VS VPS
Frequency of problems
Tremor onset PD (n=13)
Non-tremor onset PD (n=12)
Fig. 2. Mean score for each of the eight scales of the VAQ for NC,
Tremor onset PD and Non-tremor onset PD. Error bars represent
standard errors of the mean. The Non-tremor PD patients indicated
worse functioning on the light/dark adaptation, acuity/spatial vision,
depth perception, peripheral vision and visual processing speed
subscales than the NC group (p,.017). Non-tremor PD patients
also indicated worse functioning on the light/dark adaptation and
depth subscales (p,.017) than the tremor onset group. VAQ
LDA5light/dark adaptation; ASV5acuity/spatial Vision; DP5
depth perception; PV5peripheral vision; VS5visual search;
VPS5visual processing speed.
D.R. Seichepine et al.
(Allcock, Kenny, & Burn, 2006; Burn et al., 2003; Hariz et
al., 2011) and indicates that, in mild to moderate PD, visual
ADLs are preserved in the tremor subtype.
We also observed that the non-tremor subtype had worse
near contrast sensitivity when compared to either tremor
onset PD or healthy control adults. Contrast sensitivity deficits
in PD have been reported consistently (Amick et al., 2003;
Bodis-Wollner et al., 1987; Davidsdottir et al., 2008; Dieder-
ich et al., 2002; Kupersmith, Shakin, Siegel, & Liberman,
1982; Pieri, Diederich, Raman, & Goetz, 2000; Regan and
Neima, 1984; Regan and Maxner, 1987), but this is the first
study to our knowledge indicating that these deficits are
especially pronounced in the non-tremor subtype. Further
studies are needed to assess why the contrast sensitivity deficit
emerged at the near distance only. As with normal aging
and other age-related neurological disorders, the reduced sig-
nal strength stemming from deficits in visual perception may
impact cognition (Clay et al., 2009; Cronin-Golomb, Corkin,
& Growdon, 1995; Cronin-Golomb, Gilmore, Neargarder,
Morrison, & Laudate, 2007; Gilmore, Spinks, & Thomas,
2006), thereby resulting in worse functional outcomes. In PD
there is some evidence that increasing contrast improves
cognition and everyday functioning (Amick et al., 2003; Uc,
Rizzo, Anderson, et al., 2009). The results of the present
study suggest that further investigation of the effect of sensory
deficits, particularly contrast sensitivity, on cognition and
everyday function by PD subtype is warranted.
Single photon emission computed tomography studies rou-
tinely demonstrate negative correlations between striatal uptake
of dopamine and the non-tremor symptoms of PD (i.e., rigidity,
bradykinesia, gait, balance, and posture), but not tremor, sug-
gesting that the non-tremor symptoms (but not tremor) stem
from deficits in the nigrostriatal dopaminergic system. These
findings are also observed when striatal dopamine levels are
analyzed by group (i.e., non-tremor PD vs. tremor PD; Spiegel
et al., 2007). Some of the visual perceptual deficits seen in PD,
particularly contrast sensitivity, may be associated with dopa-
mine changes in the retina (for reviews, see Bodis-Wollner,
Table 2. Significant correlations between visual assessments and scores on the VAQ
CDGDLDA ASVDPPV VSVPS
Tremor onset PD
Non-tremor onset PD
.29 .21 .33
Note. For all correlations (Spearman), p,.05. CD5Color Discrimination; GD5Glare Disability; LDA5Light/Dark Adaptation; ASV5Acuity/Spatial
Vision; DP5Depth Perception; PV5Peripheral Vision; VS5Visual Search; VPS5Visual Processing Speed.
Visual ADLs in Parkinson’s disease
1990, 2009; Witkovsky, 2004). Consistent with these two lines
of investigation, we observed contrast sensitivity deficits in the
PD subtype associated with greater striatal dopamine loss (non-
tremor subtype) relative to the PD subtype with the least striatal
dopamine loss (tremor subtype). This finding suggests that the
non-tremor subtype may be associated with more significant
dopamine deficits in the retina than the tremor subtype, likely
stemming from deficits in the nigrostriatal system. Dopamine
also plays a role in visual processing in posterior cortical
regionsandithas beenproposedthat visualprocessingrelies on
a dopamine-dependent circuit between the basal ganglia and
the striate cortex (Silkis, 2007a; Silkas, 2007b). Accordingly,
contrast sensitivity deficits, especially in non-tremor onset PD,
may also stem from dopamine loss in posterior regions.
The light/dark adaption subscale of the VAQ reflects problems
performing visual ADLs that require adjusting to lighting con-
ditions, such as going from a dark movie theater into daylight.
We found that non-tremor onset PD is associated with more
problems adjusting to these settings than both a well-matched
control group and tremor-onset PD. This finding is consistent
with experimental studies indicating that patients with PD have
light adaptation (Micieli et al., 1991; Verbaan et al., 2007), but
suggest that this type of autonomic dysfunction may be more
pronounced in the non-tremor subtype. Autonomic dysfunction
as indicated by orthostatic hypotension has been previously
shown to be worse in the non-tremor subtype (Allcock et al.,
2006). Further studies exploring the extent of autonomic dys-
function by PD subtype may be warranted. It is unclear whythe
tremor onset group, unlike the other two groups, showed a
negative correlation between light–dark adaptation and acuity/
contrast sensitivity. Follow-up studies are planned to examine
Acuity and Spatial Vision
The acuity/spatial vision subscale of the VAQ reflects pro-
blems performing visual ADLs that require seeing fine detail,
such as reading small print seen in phone books or news-
papers. Three of the four items are specific to reading text that
is either small in size or of low contrast and may, therefore,
reflect difficulties with acuity and concentration. Davidsdottir
and colleagues (2005) found that over 40% of their sample of
81 PD patients reported not being able to read as well as they
used to, and they attributed these difficulties to problems with
vision and concentration. Consistent with this self-report, in
the present study we found that the scores of tremor-onset
PD patients on the acuity/spatial vision subscale correlated
with performance on contrast sensitivity (FACT). In fact, the
and contrast sensitivity was in the expected direction, with
poorer acuity/spatial behavior associated with poorer contrast
sensitivity, whereas for the other subscales the correlation
was of better acuity/spatial behavior associated with poorer
contrast sensitivity. These findings may reflect the known
individual variability of the relation between visual input and
spatial navigation in PD, with investigators attributing incon-
sistencies in the effectiveness of visual cues to compensate for
gait and postural abnormalities in PD to individual differences
atthe perceptuallevel (e.g.,Azulayetal.,1996, 1999);todate,
sample, the non-tremor subtype, but not the tremor subtype,
had significantly worse near contrast sensitivity (3.0, 6.0,
and 12.0 cpd) than the NC group. Likewise we found group
differences on the acuity/spatial subscale of the VAQ between
suggest that the worse contrast sensitivity in the non-tremor
subtype likely contributed to difficulties performing visual
ADLs involving acuity/spatial vision, particularly reading.
The depth perception subscale of the VAQ reflects problems
performing visual ADLs that require appreciating the spatial
relations between objects, such as judging the level of liquid
in a cup when pouring a cup of coffee. We found that non-
tremor onset PD was associated with more problems per-
forming depth perception related ADLs than both the NC
subtype and tremor-onset PD patients. Visuospatial deficits
in PD are well documented and have been previously linked
to side of motor symptom onset in PD (reviewed in Cronin-
Golomb, 2010), but there is only limited evidence relating
type of motor symptom to visuospatial performance.
Maeshima and colleagues (1997) reported that PD patients
with visuospatial deficits (as indicated by cube copying)
had more bradykinesia (as indicated by alternating hand
movements) than PD patients without visuospatial deficits.
Our findings are consistent with those of these investigators
in that PD patients with non-tremor onset, including those
presenting with bradykinesia, indicated more problems with
visual ADLs involving depth perception.
The peripheral vision subscale of the VAQ reflects problems
performingvisualADLs thatrequire detectingandorientingto
stimuli in the periphery, such as changing lanes in traffic due
to problems seeing cars in the next lane. Difficulties with
peripheralvision-relatedADLs inthe non-tremorsubtype may
stem from the more extensive akinesia, rigidity, and bradyki-
nesia in this group, which affect initiation and speed of
voluntary movements.Deficits inattentional systems may also
contribute to problems with peripheral vision-related ADLs.
In a series of experiments, McDowell and Harris (1997b)
examined reaction time in response to a centered visual cue
displayed on a computer monitor with and without additional
stimuli inthe periphery.Time toinitiate movement (i.e., latency
similar to that of control participants when the peripheral
field was blank (e.g., a solid color). When the peripheral field
contained additional stimuli including stationary and moving
D.R. Seichepine et al.
objects, however, PD participants were slower to initiate
movement than the control group. Follow-up experiments
indicated that this delay in motor action was particularly pro-
nounced when appearance (or disappearance) of peripheral
stimuli occurred near the onset of the visual cue that signaled
that a motor response was required. These findings are particu-
larly relevant to certain visual ADLs, such as driving, in which
stimuli in the peripheral vision are constantly changing and
require speeded motor responses. The results of the present
study indicate that non-tremor onset patients experience more
deficits with these types of visual ADLs than do healthy adults.
Visual Processing Speed
The visual processing speed scale of the VAQ assesses pro-
blems performing visual ADLs that require quickly proces-
sing visual information, such as noticing when a car directly
in front is speeding up or slowing down. Although several
studies have indicated that PD patients with an initial symp-
tom other than tremor experience worse overall cognition
than do those presenting with tremor onset (Oh, Kim, Choi,
Sohn, & Lee, 2009; Taylor et al., 2008; Verbaan et al., 2007;
Williams et al., 2007; Williams-Gray, Foltynie, Brayne,
Robbins, & Barker, 2007; Zetusky & Jankovic, 1985), ours is
the first study demonstrating a deficit in visual processing
speed that is specific to non-tremor patients.
The present study focused on the relation between visual
functioning and self-reported problems with visual ADLs in
PD subtypes, finding that the PD subtype with worse visual
functioning (non-tremor symptom onset) also endorsed more
to examine the relation between visual ADLs and cognitive
functioning. In this high-functioning sample, subgroups were
generally similar on neuropsychological performance. Further
studies using a more comprehensive cognitive assessment
with a larger sample appear warranted to determine whether
subtle cognitive deficits are related to deficits in visual ADLs.
In summary, our results indicated that PD patients with non-
tremor symptoms at disease onset, but not PD participants with
tremor at onset, had impairments in visual ADLs, particularly
those involving light/dark adaptation, acuity/spatial vision,
depth perception, peripheral vision and visual processing
speed. These findings are in accord with a growing body of
evidence that non-tremor onset PD, relative to the tremor-onset
type, is associated with more extensive cortical and subcortical
pathology as well as worse non-motor symptoms. This is the
first study to our knowledge demonstrating that the non-tremor
subtype of PD exhibits greater functional impairment when
performing visual ADLs. Environmental enhancements, such
as increasing room lighting and reducing visual clutter, may
help to ameliorate ADL impairments seen in individuals with
PD, particularly those with the non-tremor onset subtype.
We thank all of the individuals who participated in this study. Our
recruitment efforts were supported, with our gratitude, by Marie
Saint-Hilaire, MD, and Cathi Thomas RN, MSN, of Boston Medical
Center Neurology Associates, and by Boston area Parkinson Dis-
ease support groups. Karen Sullivan, PhD, collaborated on test
development. Tom Laudate, MA, Chelsea Toner, MA, Bruce Reese,
MA, and Samantha Ekka-Duffy, BA provided expert technical
support. Funding for this study was provided by the National Insti-
tute of Neurological Disorders and Stroke (R01 NS050446 and R01
NS052914 to ACG). There were no financial or other relationships
that could be interpreted as a conflict of interest affecting this article.
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