Neuropsychology © 2010 American Psychological Association

2010, Vol. 24, No. 4, 443– 456 0894-4105/10/$12.00 DOI: 10.1037/a0019279

Perceptual Bias for Affective and Nonaffective Information in Asymmetric

Parkinson’s Disease
Jared G. Smith and John P. Harris Saleem Khan
University of Reading Royal Berkshire Hospital, Reading

Elizabeth A. Atkinson and M. Susan Fowler Ralph P. Gregory

University of Reading Royal Berkshire Hospital, Reading

Objective: To relate lateralized impairments of visual perception in Parkinson’s disease to asymmetries

in the severity of motor symptoms. Method: Ten patients with worse left-sided motor symptoms
(LPD), 15 with worse right-sided (RPD), and 13 healthy age-matched controls (all right-handed) viewed
mirror-imaged pairs of emotional chimeric faces, (left side smiling, right neutral, and vice versa), of
greyscales (strips whose luminance varied smoothly from black on the left to white on the right, and vice
versa) and of gender chimeric faces (left side male, right female, and vice versa). Participants signaled
which stimulus appeared happier, brighter, or more feminine, respectively, so showing which side
received more attention. Results: For emotional chimeras, controls and LPD showed little bias, whereas
RPD showed a strong bias to left hemispace ( p ⫽ .018, r ⫽ .45). Across all patients, this bias was
associated with severity of right-sided motor impairment ( p ⫽ .018, r ⫽ .49). The bias was much weaker
and insignificant for greyscales ( p ⫽ .72, r ⫽ .14). For gender chimeras, RPD again showed a
significantly greater left hemispace bias than did LPD ( p ⫽ .037, r ⫽ .47), although neither patient group
differed significantly from controls. Across all patients, this bias correlated with ratio of right-to-left
symptom severity ( p ⫽ .044, r ⫽ .48). Conclusions: The left hemispace bias in RPD is greater for facial
than for luminance judgments, and is amplified for emotional judgments. Asymmetrical degeneration of
the striatum, particularly involving the left side, appears to underlie this deficit in visual processing.

Keywords: asymmetry, attention, chimeric faces, emotion, Parkinson’s disease

Accumulating evidence indicates that Parkinson’s disease (PD)
causes difficulties in processing emotional facial expressions (for a
review, see Assogna, Pontieri, Caltagirone, & Spalletta, 2008).
Most studies suggest that disgust is less frequently recognized in
PD, although other facial emotions, including anger, fear, surprise,
and sadness, are also affected (Clark, Neargarder, & Cronin-
Golomb, 2008; Dujardin et al., 2004; Kan, Kawamura, Hasegawa,
Mochizuki, & Nakamura, 2002; Lawrence, Goerendt, & Brooks,
2007; Sprengelmeyer et al., 2003; Yip, Lee, Ho, Tsang, & Li,
2003). Abnormalities in facial emotion recognition in PD are
assumed to arise from losses of dopaminergic neurons resulting in
dysfunction of fronto-subcortical systems and subsequent alter-
Jared G. Smith, John P. Harris, Elizabeth A. Atkinson, and M. Susan
Fowler, School of Psychology and Clinical Language Sciences, University
of Reading, Reading, United Kingdom; Saleem Khan and Ralph P. Greg-
ory, Royal Berkshire Hospital, Reading, United Kingdom.
The work reported in this article was supported by grants from the
Engineering and Physical Sciences Research Council (EPSRC) and from
the Parkinson’s Disease Society of the United Kingdom. We thank Dr.
Linda Rueckert for providing electronic versions of the original stimuli for
both the emotional and gender chimeric faces tests. We also thank the
Parkinson’s Disease Society, Dr. Jeremy Stern, and Dr. Espley for their
assistance in recruiting participants for this study and the reviewers for
helpful comments.
Correspondence concerning this article should be addressed to John P.
Harris, School of Psychology and Clinical Language Sciences, University
of Reading, Whiteknights, Reading RG6 6AL, United Kingdom. E-mail:
j.p.harris@reading.ac.uk
ation in areas strategic for the identification of specific facial
expressions, such as insula, amygdala, ventral striatum, inferior
orbitofrontal cortex, and anterior cingulate cortex (Assogna et al.,
2008; Dujardin et al., 2004; Lawrence et al., 2007; Sprengelmeyer
et al., 2003).
In recent years, interest has grown on the clinical correlates of
impaired processing of emotional facial expressions. One aspect of
the illness that has received attention concerns the relationship
between emotion recognition and side of worse motor symptoms.
In PD, the motor symptoms typically occur in an asymmetric
fashion (Hoehn & Yahr, 1967), reflecting asymmetric depletion of
dopamine in the substantia nigra, a pattern that appears to persist
across the range of disease severity (Kaasinen et al., 2001). These
changes result in asymmetrical dysregulation of the striatum, and
so asymmetrical dysfunction of multiple circuits involving the
basal ganglia and cortical regions (Marie et al., 1995; Middleton &
Strick, 2000). The asymmetric nature of the disease makes PD a
useful model in which to study the effects of subcortical degener-
ation on visuo-cognitive and emotional functions associated with
each hemisphere. Of note, studies of emotional recognition in
patients with asymmetric PD have revealed differential effects of
body side of disease onset. For example, Yip et al. (2003) found
worse recognition of all facial emotions, in particular fear and
sadness, in a large group of patients with bilateral motor symp-
toms, but noted that eight Parkinson’s patients affected only on the
right side were particularly impaired in the recognition of sadness
and disgust. More recently, Clark et al. (2008) reported that pa-
tients with left symptom onset were less accurate than controls at
identifying angry facial expressions, while patients with right

443
444 SMITH ET AL.
symptom onset were less accurate at identifying facial expressions
of surprise. This impaired facial emotion recognition was unrelated
to both severity and duration of illness, suggesting that the extent
to which dopaminergic transmission is disrupted in one hemi-
sphere or the other, rather than the overall level of dopamine
depletion, is related to PD deficits in recognition of (specific)
emotions.
One of the best studied tests of perception of facial emotion is
the chimeric faces test (Levy, Heller, Banich, & Burton, 1983).
Chimeric stimuli are stimuli in which different or discrepant in-
formation is presented in the left and right halves. In the most
common form of the test, participants are presented with two
mirror-reversed faces having differing expressions to the left and
right of the vertical midline (i.e., half of each face has a positive
expression [smiling] and the other has a neutral expression). They
then have to decide which of the two faces, overall, appeared to be
happier. Selecting the face in which the positive expression is on
the viewer’s left is interpreted as right hemisphere dominance for
the task, and vice versa for left hemisphere dominance. Previous
work has shown that right-handed healthy adults judge emotions
predominantly according to the left side of the face (Butler &
Harvey, 2008; Levy et al., 1983; Luh, Rueckert, & Levy, 1991).
Perceptual biases on these tasks have typically been accounted for
by an activation model (Kinsbourne, 1970; Luh et al., 1991), in
which selective engagement of processes subserved by either
hemisphere produces a bias for the hemispace contralateral to the
activation. Thus, because the right hemisphere is preferentially
activated by facial and/or emotional stimuli (Benton, 1990; Gur,
Skolnick, & Gur, 1994; Yovel, Tambini, & Brandman, 2008), a
contralateral (leftward) bias of attention occurs in chimeric faces,
increasing the salience of stimuli on the left. Pseudoneglect in
nonface tasks such as line bisection and greyscales (a task requir-
ing participants to make a forced two-choice discrimination of the
relative luminance of two mirror-reversed brightness gradients)
can be explained in a similar way. The small but significant left
hemispace biases in healthy participants are argued to reflect
differential engagement of right hemisphere mechanisms for pro-
cessing complex visuospatial stimuli and/or attentional control
(Fink et al., 2000; Jewell & McCourt, 2000; Mattingley, Brad-
shaw, Nettleton, & Bradshaw, 1994; Nicholls, Bradshaw, & Mat-
tingley, 1999).
The chimeric faces test holds much appeal as a method to
explore emotional processing in PD because the task yields reli-
able individual differences in perception (Levy et al., 1983; Rueck-
ert, 2005). Furthermore, patterns of attentional asymmetry on
chimeric tests have been shown to be highly sensitive to unilateral
hemispheric damage, as in stroke (Mattingley et al., 1994). Al-
though little work using chimeric stimuli has been conducted in
patients with PD, an accumulating literature has provided compel-
ling evidence for lateralized perceptual bias in patients with PD on
range of visuospatial tasks without a facial or affective component
(Ebersbach et al., 1996; Harris, Atkinson, Lee, Nithi, & Fowler,
2003; Lee, Harris, Atkinson, & Fowler, 2001; Starkstein, Lei-
guarda, Gershanik, & Berthier, 1987). In general, patients who
suffer from motor symptoms predominantly on their left side
(LPD), thought to reflect a greater loss of dopamine in the right
basal ganglia, appear to be more vulnerable to perceptual asym-
metries than patients with greater dopamine loss in the left basal
ganglia whose symptoms are predominantly on their right side
(RPD). For example, in two early studies, LPD groups exhibited
signs of left spatial neglect in line bisection and tasks involving
saccades to a target in the face of near-normal performance in RPD
(Starkstein et al., 1987; Ventre, Zee, Papageorgiou, & Reich,
1992). In a later study of horizontal line bisection, which involved
adjusting the position of a cursor on a large screen with remote
switches, RPD patients and controls both evidenced pseudoneglect
(a mild left hemispace bias), whereas LPD patients demonstrated
left hemispatial neglect (i.e., bisected lines to the right of the
midpoints), a bias that was small but nonetheless significant (Lee
et al., 2001). Subsequent work by the same group revealed that
identical rectangles are perceived by LPD patients as narrower
when presented in left hemispace, offering further support to the
idea that dopamine is especially important in the representation of
the left visual field (Harris et al., 2003). Davidsdottir, Wagenaar,
Young, and Cronin-Golomb (2008) recently presented evidence
for a lateralized deficit in optic flow perception in PD. In this
experiment, control subjects and PD patients with right-symptom
onset perceived optic flow in their left hemifield as moving faster
than flow in the right hemifield, while patients with left-symptom
onset exhibited an opposite trend.
Together then, this evidence suggests at least a small but reliable
left-neglect syndrome in LPD on visuospatial tasks. Attentional
deficits associated with neglect may be expected in LPD patients,
given links between visuospatial performance and the right parietal
lobe to which dopaminergic neurons project via basal ganglia-
thalamocortical circuitry (Clower, Dum, & Strick, 2005; Fimm et
al., 2001; Fink et al., 2000). Nevertheless, it should also be noted
that (right-sided) inattention can occur following right-sided dam-
age confined to subcortical areas affected by PD, most critically
the putamen and the caudate nucleus (Karnath, Himmelbach, &
Rorden, 2002). Furthermore, some studies have reported selective
visuospatial impairments in RPD patients (Cooper et al., 2008;
Davidsdottir et al., 2008), while double dissociations for LPD and
RPD groups have been reported on visuospatial tasks such as hand
rotation (Amick, Schendan, Ganis, & Cronin-Golomb, 2006) and
tests of hierarchical pattern perception requiring local or global
processing (Schendan, Amick, & Cronin-Golomb, 2008). There-
fore, patients with PD, with predominantly right-sided symptoms
can exhibit disrupted visuospatial processing, and, under some
circumstances, even opposite visuospatial impairments from their
left-sided counterparts. These impairments may have implications
for errors in direction of gait, an issue to which we return in the
General Discussion.
In the present study, we investigated in PD and controls facial
emotion-based and nonfacial tasks that typically yield visuospatial
field biases. Correlations between the emotional chimeric faces test
and nonfacial or visuospatial tasks that measure perceptual asym-
metries (e.g., greyscales, line bisection), are quite low, suggesting
they engage a similar but not identical set of cognitive and neural
mechanisms (Luh et al., 1991; Mattingley et al., 1994; Nicholls et
al., 1999). It is important to note that the degree to which the right
hemisphere is dominant in healthy participants’ performance on
the emotional chimeric faces test has been shown to be linked to
measures of emotional awareness, including the ability to interpret
facial expressions of emotion, suggesting that emotional chimeric
faces tests likely measure individual differences in right hemi-
sphere mechanisms underlying affective recognition, superim-
posed upon a right hemisphere specialization for processing visuo-
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE
spatial information (Kim, Levine, & Kertesz, 1990; Rueckert &
Naybar, 2008; Rueckert & Pawlak, 2000). Functional brain imag-
ing has shown that, in control participants, regions affected by PD,
such as the basal ganglia and frontal cortex, are preferentially
responsive during facial affect recognition (Kan et al., 2002;
Sprengelmeyer et al., 2003). Thus, comparing LPD and RPD
patients’ responses with chimeras could provide insight into how
asymmetric dopaminergic transmission in PD affects cerebral lat-
eralization of affective facial and nonfacial information. If a par-
ticular subgroup has greater difficulties in identifying facial
expressions, they are likely to have more difficulties in social
interaction, and so need more targeted information and advice
from clinicians.
Experiment 1: Emotional Chimeric Faces
and Greyscales
Introduction
In the present study, we examined whether PD patients would
demonstrate atypical perceptual biases for emotion-based facial
and nonfacial chimeras related to the side of worse motor impair-
ment. Studies of both facial expression recognition and (lateral-
ized) visuospatial function have shown differences in PD related to
side of motor symptom onset (Clarke et al., 2008; Davidsdottir et
al., 2008; Ebersbach et al., 1996). Based on these findings, it was
hypothesized that relative to RPD patients, LPD patients would
evidence a decreased left spatial bias across tasks, although this
effect would be heightened in the test of emotional chimeric faces,
given the specific disturbance of recognition of facial emotion
expressions in PD patients (Assogna et al., 2009; Clark et al.,
2008). In addition to group comparisons of LPD and RPD patients,
we investigated whether severity of left- or right-sided symptoms
(irrespective of which were worse) was related to perceptual
asymmetries. Finally, because impairments in decision-making
and categorization may occur in PD (Filoteo, Maddox, Ing, &
Song, 2007), and discrimination or identification of facial expres-
sions may be related to cognitive impairment (Dujardin et al.,
2004; Yip et al., 2003), a battery of neuropsychological tests was
also run, to measure any deficits in memory and executive func-
tions, and so allow assessment of the potential influence of im-
paired cognition.
Method
Participants. Twenty-five patients with idiopathic PD and 13
age-matched healthy controls participated in the experiment. All
were screened for dementia using the Mini-Mental State Exami-
nation (MMSE cut-off ⫽ 24, Folstein, Folstein, & McHugh, 1975)
and for depression using the Beck Depression Inventory-II (BDI-II
cut-off ⫽ 17, Beck, Steer, & Brown, 1996). All were right-handed
as assessed by the Edinburgh Handedness Inventory (Oldfield,
1971). None had a history of head injury within the preceding 10
years, or of alcohol abuse, stroke, or epilepsy, and all had normal
or corrected-to-normal vision. The diagnosis of idiopathic PD was
confirmed by a consultant neurologist and all patients met U.K.
Parkinson’s disease Brain Bank Criteria for diagnosis of PD (Gibb
& Lees, 1988). Ethical approval was given by the Berkshire Local
Research Ethics Committee, and by the University of Reading
445
Research Ethics Committee. All participants gave their informed
consent after a verbal and a written description of what their
participation would involve.
Clinical assessment. The Unified Parkinson’s disease Rating
Scale Motor subscale (UPDRSm; Fahn, Elton, & Members of the
UPDRS Development Committee, 1987) was used as a measure of
current motor severity in patients with PD and to classify patients
into left- and right-sided PD groups. Patients were evaluated by a
consultant neurologist blind to experimental results 45 to 75 min
after administering their usual PD medication (when the patient
was in an “ON” state), and so in the same state as when the
experimental tasks were performed. One patient was unavailable
for motor function examination, and so was classified as LPD from
the side of first symptom onset. For the assessment, right- and
left-sided motor composite scores were created by summing the
individual UPDRS motor subscale items of tremor (items 20 and
21), rigidity (item 22) and bradykinesia (items, 23, 24, 25, and 26).
Degree of asymmetry of motor dysfunction for each participant
was determined by calculating a motor asymmetry score using the
left and right motor composite scores obtained from patients:
(UPDRSm Right – UPDRSm Left)/(UPDRSm Right ⫹ UPDRSm
Left). This formula gives a result of zero when left and right motor
scores are equal, a negative number when left symptoms are
worse, and a positive number when right symptoms are worse.
Based on these scores, patients were divided into two groups, those
with motor symptoms predominantly on the left (LPD, n ⫽ 10),
and those with symptoms predominantly on the right (RPD, n ⫽
15). LPD asymmetry scores ranged from ⫺0.07 to ⫺0.40 and RPD
scores from 0.06 to 1.00.
The demographic and clinical characteristics of the subgroups
are shown in Table 1. There was a high number of men in the RPD
group (12/15) compared with both the LPD (5/10) and control
groups (6/13), which tended to have an equal balance of men and
women. Nevertheless, Fisher’s exact tests revealed nonsignificant
differences between the PD subgroups ( p ⫽ .189) and between
RPD and controls ( p ⫽ .114). The subgroups were, generally
speaking, well matched on age and education, and two-tailed t tests
(comparing each pair of experimental groups) revealed no signif-
icant differences between groups on these variables, although there
was a trend for RPD patients to be more educated than their LPD
counterparts ( p ⫽ .083). Although BDI-II scores were elevated in
each of the patient subgroups relative to controls, the scores of the
PD subgroups were comparable with each other and within the
normal range.
The PD subgroups were also matched on variables related to
their illness, including disease severity and medication regimes. As
assessed by the Hoehn and Yahr (1967) degree of clinical disabil-
ity scale, 2 (LPD) patients were in Stage I, 15 patients (5 LPD, 10
RPD) were in Stage II, 7 patients (3 LPD, 4 RPD) were in Stage
III, and 1 (RPD) patient was in Stage IV. There were no significant
differences between the subgroups with respect to mean stage of
illness, disease duration and total UPDRSm. Unsurprisingly, left-
sided UPDRSm scores were higher in LPD patients than RPD
patients, while motor symptoms on the right-side of the body were
more severe in RPD than LPD patients. Motor asymmetry scores
were also significantly different between the RPD and LPD
groups, reflecting RPD participants’ scores that were positive and
LPD participants’ scores that were negative. Although the RPD
group evidenced a numerically larger degree of asymmetry than
446 SMITH ET AL.

Table 1
Demographic, Clinical, and Neuropsychological Performance Data for Predominantly Left-Sided Parkinson’s Patients (LPD),
Predominantly Right-Sided Parkinson’s Patients (RPD), and Control Participants
M (SD) t

Patients With LPD Patients With RPD Controls LPD vs. LPD vs. RPD vs.
Measure (n ⫽ 10) (n ⫽ 15) (n ⫽ 13) RPD Control Control

Age (years) 65.62 (6.63) 70.39 (6.93) 67.01 (5.25) ⫺1.72 ⫺.562 1.44
Education (years) 11.65 (2.11) 13.33 (2.38) 12.15 (2.45) ⫺1.81 ⫺.518 1.29
Hoehn & Yahr stage (“ON”) 2.30 (0.67) 2.60 (0.54) ⫺1.23
Disease duration (years) 7.10 (4.60) 5.70 (4.43) 0.76
UPDRSm “ON”a 18.56 (3.28) 20.27 (6.42) ⫺0.86
UPDRSm right-sided symptoms “ON” 5.11 (1.76) 8.53 (3.42) ⴚ2.77ⴱ
UPDRSm left-sided symptoms “ON” 7.33 (1.12) 4.67 (3.06) 3.05ⴱⴱ
Motor Asymmetry score ⫺0.20 (0.14) 0.36 (0.30) ⴚ6.05ⴱⴱⴱ
BDI-II 9.20 (3.82) 8.67 (4.14) 5.00 (3.22) 0.33 2.91ⴱⴱ 2.62ⴱ
MMSE 28.70 (1.06) 28.20 (1.21) 28.77 (1.09) 1.06 ⫺0.15 ⫺1.30
NART 114.22 (7.56) 120.14 (8.22) 114.66 (8.14) ⫺1.82 ⫺0.13 1.77
COWAT 43.60 (12.45) 39.53 (14.19) 40.46 (10.40) 0.74 0.66 ⫺0.19
ANT 21.70 (3.56) 22.20 (5.74) 25.46 (5.74) ⫺0.25 ⫺1.82 ⫺1.50
CERAD Total trials 1–3 (0–30) 18.60 (5.04) 16.47 (3.44) 21.31 (2.96) 1.26 ⫺1.62 ⴚ3.96ⴱⴱⴱ
CERAD Delayed Recall (0–10) 5.20 (1.93) 4.67 (1.84) 6.38 (1.76) 0.70 ⫺1.54 ⴚ2.52ⴱ
Stroop A 82.10 (16.74) 79.33 (11.58) 84.77 (15.16) 0.49 ⫺0.40 ⫺1.07
Stroop B 38.30 (13.58) 43.80 (8.52) 45.69 (15.89) ⫺1.25 ⫺1.18 ⫺0.40
Stroop A ⫺ Stroop B 43.80 (9.52) 35.53 (12.44) 39.08 (11.03) 1.78 1.08 ⫺0.79
TMTA 49.92 (15.38) 46.29 (16.79) 37.64 (18.60) 0.55 1.69 1.29
TMTB 172.98 (103.23) 120.90 (35.49) 125.77 (105.05) 1.54 1.08 ⫺0.16
TMTB ⫺ TMTA 123.06 (98.13) 74.61 (31.80) 88.13 (11.03) 1.51 0.88 ⫺0.50

Note. UPDRSm “ON” ⫽ Score on motor subscale of Unified Parkinson’s Disease Rating Scale post administration of medication; Motor asymmetry
score ⫽ (UPDRSm Right ⫺ UPDRSm Left)/(UPDRSm Right ⫹ UPDRSm Left); MMSE ⫽ Mini Mental Status Examination; BDI-II ⫽ Beck Depression
Inventory II; NART ⫽ National Adult Reading Test (expressed as a Wechsler Adult Intelligence Scale–Revised Full Scale equivalent); COWAT ⫽
Controlled Oral Word Association Test; ANT ⫽ Animal Naming Test; CERAD ⫽ wordlist memory test from the Consortium to Establish a Registry for
Alzheimer’s Disease battery; TMT ⫽ Trail Making Test.
a
One patient with LPD did not partake in UPDRS motor assessments.
ⴱ
p ⬍ .05. ⴱⴱ p ⬍ .01. ⴱⴱⴱ p ⬍ .001. Significant t values are shown in boldface.

the LPD group, a comparison of the absolute values of group
motor asymmetry scores revealed that this difference was not
statistically significant, F(1, 23) ⫽ 2.24, p ⫽ .149. At the time of
testing all 25 patients with PD were receiving anti-parkinsonian
medication and were in an “ON” phase. Specifically, three of the
(RPD) patients were receiving levodopa (Stalevo, Sinemet and/or
Madopar) exclusively, while 7 patients (3 LPD, 4 RPD) were
taking dopamine agonists (Mirapexin, Ropinerole, or Pergolide)
exclusively. Eleven of the patients (5 LPD, 6 RPD) were taking
both levodopa and agonist medication, of which 3 (LPD patients)
were also receiving Amantadine. In addition to dopamine ago-
nists, 1 RPD patient was also taking a MAO-B inhibitor (Rasagi-
line) while 1 LPD patient was also receiving anticholinergic med-
ication (Trihexphenidyl). Finally, 1 LPD patient who was receiv-
ing levodopa was also taking a MAO-B inhibitor (Selegeline) and
Amantadine and 1 RPD patient undergoing levodopa treatment
was also being administered both a MAO-B inhibitor (Selegeline)
and a COMT inhibitor (Entacapone). Fisher’s exact tests indicated
that the PD subgroups were not significantly different in the
proportion of participants treated with levodopa medication (LPD:
6/10, RPD: 10/15, p ⫽ .999) or dopamine agonists (LPD: 9/10,
RPD: 11/15, p ⫽ .615). One LPD patient was also receiving SSRI
antidepressant medication (Fluoxetine).
Aspects of basic visual function were assessed as follows in all
but two of the patients (9/10 LPD; 14/15 RPD). Visual acuity was
measured in each eye with the Times Roman Reading Charts of the
MaclureTest (Clement Clarke International Ltd.), on which the
ability to read a type size of N6 at the normal reading distance
corresponds approximately to a Snellen Acuity of 6/6. Taking
acuity in the worst eye when the eyes were not equal, the mean
acuity of the LPD group was N5.67 (range ⫽ N5–N8), while all
patients in RPD group read at N5. Two tests of stereopsis were also
run. On the Randot test of stereopsis, the scores were: LPD M ⫽
119.88s (SD ⫽ 194.85, range ⫽ 20 – 600); RPD M ⫽ 84.64s
(SD ⫽ 60.08, range ⫽ 20 –200). On the TNO test of stereopsis, the
scores were: LPD M ⫽ 506.67s (SD ⫽ 837.78, range ⫽ 30 –1980);
RPD M ⫽ 299.21s (SD ⫽ 258.31, range ⫽ 60 –1860). In a group
of healthy elderly individuals, mean scores on the Randot test of
45s and on the TNO test of 275s were found (Fowler, 1996). In a
group of normal participants, whose ages ranged from 4 to 74
years, a mean Randot score of 44s and a mean TNO score of 194s
were found (Mazow, Prager, & Cathey, 1983). Thus, although they
were somewhat impaired on the Randot test, both patient groups
clearly retained some stereoscopic vision. On clinical examination,
all patients except one RPD patient (bilateral restriction of eleva-
tion) showed the full range of ocular movements. One patient in
the LPD group and two in the RPD group showed a small hy-
pometria of saccades (left ⬎ right). Pursuit eye-movements were
sometimes jerky in four patients in the LPD group and 10 patients
in the RPD group. All patients could converge on a near point
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE 447

of 20 cm or less except for one LPD patient (30 cm) and 2 RPD
patients (30 cm, 40 cm). Thus, we conclude that the patients were
not suffering from gross disorders of acuity or binocularity
which would interfere with their perception of chimeric faces or
greyscales.
Neuropsychological assessment. All participants were ad-
ministered a small battery of neuropsychological tests, which
included the National Adult Reading Test (NART; Nelson &
Willeson, 1991) as well as measures of verbal fluency, specifically,
the Controlled Oral Word Association Test (COWAT; Benton &
Hamsher, 1976) and the Animal Naming subtest from the Boston
Diagnostic Aphasia Examination (ANT; Goodglass & Kaplan,
1972). Participants also performed the Stroop task and the Trail
Making Test, while verbal memory was assessed using the
wordlist memory test from the CERAD battery (Consortium to
Establish a Registry for Alzheimer’s disease; Rosen, Mohs, &
Davis, 1984). A summary of the neuropsychological test results is
displayed in Table 1. Differences across all experimental groups
were generally small and mostly nonsignificant with the notable
exception of CERAD, on which controls outperformed both pa-
tient subgroups, although significantly so only compared to RPD
participants. Similarly, t tests comparing the PD subgroups against
each other showed comparable performance on the MMSE, mea-
sures of verbal fluency and CERAD recall ( p ⬎ .10). However,
NART performance was marginally better in RPD patients than in
LPD patients ( p ⫽ .082). Although the cost of incongruent color-
word condition on the Stroop and task switching on the Trail
Making Test was numerically greater for LPD than RPD patients,
suggesting mildly impaired executive abilities in the LPD group,
differences were not significant on either task.
Materials and procedure. Experimental stimuli were the
emotional chimeric faces test and the greyscales task, presented in
a counterbalanced order within each subject group. Both experi-
mental conditions were run on an IBM compatible PC with stimuli
presented on a 410 ⫻ 350 mm monitor at XVGA (1600 ⫻ 1200
pixel) resolution. Throughout the testing period, participants were
encouraged to align their midlines with the center of the display
and to remain as still as possible. Experimental stimuli were
viewed from a distance of approximately 57 cm. In each task,
participants were requested to examine stimuli carefully, and were Figure 1. Example of a chimeric face in the emotional chimeric faces
permitted to respond without time constraints. test. The participants’ task is to decide which of the two faces looks,
Emotional Chimeric Faces Test. Participants were adminis- overall, happier. Here the top face is expressing positive emotion in the left
tered a computerized version of the Levy et al. (1983) emotional visual field and the bottom face is expressing positive emotion in the right
chimeric faces task in which the 36 stimuli had been scanned and visual field. From “Asymmetry of perception in free viewing of chimeric
saved as gif files (for a Web version of this computerized version, faces,” by J. Levy, W. Heller, M. T. Banich, & L. A. Burton, 1983, Brain
see Rueckert, 2005). Each of the stimuli was defined by a thin and Cognition, 2, p. 406. Reproduced with permission.
black rectangle against a white background and subtended a retinal
angle of about 12.7 degrees (deg) high ⫻ 9.7 deg wide. The
horizontal and vertical midlines of the stimulus pairs were aligned in a matched set of four pairs of chimeric stimuli from each poser,
with the center of the display window. Details on construction of yielding a total of 36 stimulus pairs. The counterbalancing of
the chimeric face stimuli have been provided elsewhere (Levy et stimuli ensured that any consistent response bias (e.g., always
al., 1983). Briefly, this involved photographing twice each of nine choosing the top face) would result in a mean bias of zero. The 36
posers, once with a smiling and once with a neutral expression and trials were arranged in a pseudorandom order whereby trials were
joining the vertical halves of each together to form a chimeric face divided into four randomly ordered blocks of nine trials. Each
(i.e., a left-side smiling face was paired with a right-side neutral block consisted of one stimulus pair from each poser (four/five of
face or a right-side smiling face was paired with a left-side neutral these pairs presented the top stimulus with the smiling face on the
face). Each chimera was then paired with its mirror image. An left side and the bottom stimulus with the smiling face on the right
example of a pair of chimeras is provided in Figure 1. The vertical and five/four trials vice versa). Subjects were asked to indicate
position of each member of a pair was counterbalanced, resulting which of the two faces looked happier overall by pressing one of
448
two spatially compatible, brightly colored response buttons labeled
“upper” and ‘lower.’ The response panel was placed in such a way
that the push-buttons were spatially compatible with the stimuli
(i.e., the “upper” button above the “lower” button) and was aligned
centrally with respect to the monitor. To eliminate the potential
effects of lateralized motor response bias in PD patients (arising
from, e.g., hemispatial akinesia), participants indicated their deci-
sions in both tasks by using both index fingers to press the
appropriate response button. Participants were watched carefully
by an experimenter to ensure responses were made in this manner.
In between each response, participants rested their index fingers on
a white strip placed horizontally on the response panel between the
two buttons. After a response, the display was cleared and a new
trial began after an interstimulus period of 1500ms. No feedback
was provided. Three practice trials were administered prior to
performance of the chimeric faces test.
Greyscales task. Participants performed the computerized
greyscales task of Nicholls et al. (1999) and made available by the
authors at http://www.psych.unimelb.edu.au/research/laterality/
greyscales.html. In each of 72 trials, participants made a forced
two-choice discrimination of the relative brightness of two verti-
cally aligned gradients presented simultaneously. Each of the
stimuli was defined by a thin black rectangle against a gray
background and was 3 deg high. To discourage the use of a
standard response, the length of the gradients was varied be-
tween 12.2, 15.3, 18.3, 21.4, 24.4, and 27.5 deg (12 trials for each
stimulus length). The horizontal and vertical midlines of the stim-
ulus pairs were aligned with the center of the display window. The
gradients changed incrementally from white on one side to black
on the other and were arranged so that they were left/right rever-
sals of each other (for a detailed description of how changes in
gradient brightness were achieved, see Nicholls et al., 1999). Thus,
if the upper stimulus was darker on the right, the lower stimulus
was darker on the left (see Figure 2 for an example). Participants
were asked to indicate which of the two gradients comprising each
stimulus appeared darker overall in the same manner as in the
emotional chimeric faces test. The greyscales program presented
the different factorial combinations of length and stimulus orien-
tation in a pseudorandom order. As before, the interstimulus in-
Figure 2. Example of a stimulus from the greyscales task. Participants
were required to indicate which of the two rectangles appeared overall the
darker. The axis of the required response (top/bottom) is orthogonal to the
axis of any attentional bias (left/right), thus avoiding the possible effects of
motor response bias. From “Freeviewing perceptual asymmetries for the
judgement of brightness, numerosity and size,” by M. E. R. Nicholls, J. L.
Bradshaw, & J. B. Mattingley, 1999, Neuropsychologia, 37, p. 308. Re-
produced with permission.
SMITH ET AL.
terval was 1,500ms and no feedback was provided. Six practice
trials were given before the greyscales task.
Results
Measures of perceptual bias. Responses were categorized
according to whether they selected the stimulus with the salient
feature on the left or right side irrespective of whether it was the
upper or lower stimulus. For the emotional chimeric faces task, a
response was defined as left-biased if the participant selected the
chimera with the left-side smiling face and right-biased if they
selected the right-side smiling face. Similarly, for the greyscales
task, responses to each stimulus were categorized as left-biased or
right-biased according to whether the participant had chosen the
rectangle with the darker end on the left or right. An asymmetry
score for each test was derived by subtracting the number of left
choices from the number of right choices, and dividing the result
by the total number of items (36 in emotional chimeric faces, 72 in
greyscales; see Mattingley et al., 1994).
The mean asymmetry scores of each group for emotional chi-
meric faces and greyscales are shown in Figure 3. Although the
three groups showed negative asymmetry scores, suggesting a left
hemispace bias for both tasks, the negative asymmetry scores of
RPD patients were larger than those of either the LPD or control
groups, most obviously on the emotional chimeric faces test. These
observations tended to be confirmed in statistical analyses.
Whereas the emotional chimeric faces asymmetry scores of both
LPD patients (M ⫽ ⫺0.06, SD ⫽ 0.53) and control subjects (M ⫽
⫺0.07, SD ⫽ 0.48) were not significantly different from zero ( p ⬎
.5), RPD patients exhibited a highly significant left hemispace bias
for chimeras, (M ⫽ ⫺0.53, SD ⫽ 0.43, t(14) ⫽ ⫺4.84, p ⬍ .001,
r ⫽ .79). A one-way analysis of variance (ANOVA) of asymmetry
scores for the three groups confirmed a significant effect of group
on the emotional chimeric faces test, F(2, 35) ⫽ 4.49, p ⫽ .018,
MSE ⫽ 0.22, r ⫽ .45, reflecting the greater left hemispace bias in
RPD patients compared with the other experimental groups. This
effect remained when demographic (gender, years of education)
and clinical (BDI-II scores) variables and neuropsychological per-
formance (Wechsler Adult Intelligence Scale [WAIS] Full IQ;
Consortium to Establish a Registry for Alzheimer’s Disease
[CERAD] total and delayed recall), measures for which there were
differences (or suggested differences) across experimental groups,
were factored in as covariates, F(2, 29) ⫽ 3.52, p ⫽ .043,
MSE ⫽ 0.23, r ⫽ .41. Post hoc tests (two-tailed t tests) indicated
that RPD patients had a greater left hemispace bias when com-
pared with either LPD patients ( p ⫽ .021, r ⫽ .46) or controls
( p ⫽ .011, r ⫽ .47), but there was no significant difference
between LPD patients and controls.
In the greyscales task, RPD patients once again showed a strong
left hemispace bias, M ⫽ ⫺0.41, SD ⫽ 0.36, t(14) ⫽ ⫺4.32, p ⬍
.001, r ⫽ .76, indicating that they predominantly selected as darker
the rectangle in which the black end appeared on the left. In
contrast, control subjects showed only a marginally significant left
hemispace bias, M ⫽ ⫺0.29, SD ⫽ 0.53, t(12) ⫽ ⫺1.95, p ⫽ .075,
r ⫽ .49, while LPD patients mean asymmetry score just missed
significance, M ⫽ ⫺0.29, SD ⫽ 0.42, t(9) ⫽ ⫺2.23, p ⫽ .052, r ⫽
.60. However, although the RPD group showed a numerically
larger left hemispace bias than did LPD and control participants,
there was no significant effect of group for this task, F(2,
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE
0
-0.1
-0.2
Asymmetry Score
-0.3
-0.4
-0.5
-0.6
-0.7
-0.8
Figure 3. Mean asymmetry score on the emotional chimeric faces test and the greyscales task for predominantly
left-sided Parkinson’s patients (LPD), predominantly right-sided Parkinson’s patients (RPD), and control participants.
Negative scores indicate a leftward bias for chimeras. Error bars represent the standard errors of the mean.
35) ⫽ 0.33, p ⫽ .719, r ⫽ .14. Correlational analyses performed
separately on data from each subject group revealed that there
were no significant relationships between scores on the greyscales
and chimeric faces tasks, LPD: r(10) ⫽ .57, p ⫽ .088; RPD:
r(15) ⫽ ⫺.01, p ⫽ .978; Controls: r(13) ⫽ .22, p ⫽ .470.
Visuospatial impairments have been related to symptom sever-
ity on one side of the body irrespective of severity on the other side
(Cooper et al., 2008). Therefore, the relationship between severity
of left- and right-sided symptoms and asymmetry scores on the
emotional chimeric faces and greyscales tasks was investigated
using separate linear regression analyses (that considered all pa-
tients with PD as one group) with asymmetry scores on each
experimental task as the dependent variable and UPDRS scores for
left- and right-sided motor symptoms as the independent variable.
This showed that left-sided motor symptoms were not significantly
related to perceptual bias for emotion-based facial or nonfacial
stimuli: emotional chimeric faces, R2 ⫽ 0.246, ␤ ⫽ ⫺.010, t(23) ⫽
⫺0.05, p ⫽ .961; greyscales, R2 ⫽ 0.131, ␤ ⫽ ⫺.044, t(23) ⫽
⫺0.21, p ⫽ .833. But there was a significant association of
right-sided motor impairment with emotional chimeric faces,
R2 ⫽ 0.246, ␤ ⫽ ⫺.494, t(23) ⫽ ⫺2.57, p ⫽ .018. This indicates
that, across PD patients, more severe right-sided motor symptom-
atology was linked with increased left hemispace bias on the
emotional chimeric faces test. This effect remained after control-
ling for gender, years of education, and WAIS Predicted Full-Scale
IQ (the measures for which there were suggested differences
between patient subgroups), R2 ⫽ 0.488, ␤ ⫽ ⫺.434, t(23) ⫽
⫺2.46, p ⫽ .024. The relationship between right symptoms and
lateralized scores on greyscales failed to reach significance, how-
ever, R2 ⫽ 0.131, ␤ ⫽ ⫺.351, t(23) ⫽ ⫺1.70, p ⫽ .104.
Post hoc analyses (pairwise correlations) showed that overall
UPDRS motor score was only weakly associated with asymmetry
scores (presumably reflecting the relationship between bias and
severity of right-sided symptomatology rather than disease sever-
ity per se), with neither correlation significant: emotional chimeric
faces, r(23) ⫽ ⫺.34, p ⫽ .109; greyscales, r(23) ⫽ ⫺.23, p ⫽
.289. Further, there was no association of either test score with
ratio of left-to-right symptoms, duration of illness, or any other
449
LPD
RPD
Control
clinical or demographic measure ( p ⬎ .10) while asymmetry
scores of PD patients were also not significantly predicted by
performance on any administered neuropsychological measure
( p ⬎ .05), suggesting that perceptual bias in (right-sided) PD
participants was not related to cognitive functioning (e.g., mne-
monic and executive abilities).
Discussion
The findings from Experiment 1 were, at least to some extent,
unexpected. While, as predicted, LPD patients displayed decreased
left hemispace bias relative to RPD, LPD patients were similar to
controls on both tasks. Rather, RPD patients showed abnormal
asymmetry, most obviously in the chimeric faces test, perhaps
indicative of a left hemispace bias for facial affect. Further, irre-
spective of side of worse symptoms, there was a significant rela-
tionship between asymmetry scores for emotional chimeric faces
and right-sided motor impairments in all patients. Although similar
to that of a recent study in which visuospatial deficits were asso-
ciated with right-sided symptoms and not left (Cooper et al., 2008),
this association remains counterintuitive, given suggestions that
the right hemisphere is the director of emotion processing, facial
recognition and visuospatial cognition (Fink et al., 2000; Gur et al.,
1994; Kinsbourne, 1970; Yovel et al., 2008).
It is noteworthy that the association between severity of right-sided
PD symptomatology and leftward attentional bias was only observed
in the emotional chimeric faces test and group differences in asym-
metry scores were significant only in this test (and not greyscales).
Also, the association between asymmetry scores in RPD on chimeric
faces and greyscales tasks was close to zero, indicating that the degree
of left hemispace bias exhibited by each patient in one test was
independent of that in the other. One possibility is that the chimeric
faces test is a more sensitive measure of attentional bias than grey-
scales in PD, and these findings reflect a genuine right-hemisphere
bias in RPD, possibly indicative of abnormal left parieto-temporal
function. Models of cerebral lateralization have proposed that the
lateralization of a number of subprocessors gives rise to perceptual
asymmetries which differ across different tasks. Thus, judgments of
450 SMITH ET AL.

emotional content of faces and of brightness would each engage a smaller monitor (340 ⫻ 270 mm) although still at XVGA (1600 ⫻
unique set of subprocessors, leading to differences in patterns of 1200 pixel) resolution. As before, participants’ responses were
attentional bias and thus the observed perceptual asymmetries (Ni- recorded using the same vertically aligned, brightly colored, two-
cholls et al., 1999). In support of this approach, Mattingley and button response panel interfaced with the PC.
colleagues (1994) reported that despite a significant right hemispace Participants were administered a computerized gender chimeric
bias on both chimeric faces and greyscales in patients with right faces task used by Luh et al. (1991) in which the same 12 stimuli had
hemisphere damage after stroke, and a significant left hemispace bias been scanned and saved as gif files. As previously, each of the stimuli
on both tasks in controls, the sizes of directional biases within each was defined by a thin black rectangle against a white background and
group were not related. Thus we may not need to look beyond deficits was 12.7 deg high ⫻ 9.7 deg wide. The horizontal and vertical
in attention or visuospatial cognition to explain the small intratask midlines of the stimulus pairs were aligned with the center of the
correlations in Experiment 1. display window. Details of the construction of the gender chimeric
Choosing the chimeric face that looks happier almost certainly face stimuli have been provided elsewhere (Luh et al., 1991). Briefly,
involves emotional processes not active in greyscales, and so the this involved photographing four times each of six posers, three males
exaggerated left hemispace bias in RPD may reflect a deficit in and three females, and joining the vertical halves of one male with one
comprehending emotional facial cues. There is increasing evidence female to form a chimeric face (i.e., a left-side male face was paired
that it is the left rather than the right hemisphere that mediates positive with a right-side female face or a right-side male face was paired with
emotions (Fusar-Poli et al., 2009; Gur et al., 1994; Root, Wong, & a left-side female face). Each chimera was then paired with its mirror
Kinsbourne, 2006), and recent work has suggested that, after control- image (see Figure 4 for an example). The vertical position of each
ling for depression, RPD patients are more likely than LPD patients to
view expressions with an ambiguous valence (e.g., surprise) in a more
negative light (Clark et al., 2008). While the happy chimeras in the
Levy et al. (1983) task used here were not intended to be ambiguous,
significant disruption to left hemisphere function in RPD may have
resulted in perception of emotions different from that in LPD and controls
which, in turn, could have affected judgments of facial chimeras.
To address this possibility, and to better characterize the later-
alized performance of LPD and RPD patients on chimeric stimuli,
a second experiment was conducted using a chimeric faces test in
which the faces have a neutral expression and the task does not
involve judgment of emotional content. This was the gender chi-
meric faces test, a brief test developed in the early 1990s by the
Levy group (Luh et al., 1991). This seemed an appropriate measure
since PD does not appear to disrupt the facial perception of gender
(Sprengelmeyer et al., 2003).

Experiment 2: Gender Chimeric Faces

Introduction
To check the possible role of emotion in Experiment 1, a chimeric
faces test was run which required decisions about the perceived
gender of faces rather than their emotional content. If asymmetric
illness disrupts visuospatial processing of facial stimuli, then RPD
patients should exhibit a greater preference for the face on the left.
However, if the abnormal perceptual bias in (R)PD patients does not
entail processing of affective information, then performance in RPD
should be comparable with that of LPD and control participants.

Materials and Methods

Participants. The same participants took part as in the previ-
ous experiment, less 4 RPD patients, 1 LPD patient, and 1 control
participant, who were not available. This left 11 RPD patients (1
woman, 10 men); 9 LPD patients (4 women, 5 men) and 12 control
participants (6 women, 6 men).
Materials and procedure. The experimental apparatus was
identical to the previous experiment with one exception; the gen-
der chimeric faces task was performed using a different IBM
compatible PC. In this instance, stimuli were presented on a
Figure 4. Example of a chimeric face in the gender chimeric faces test.
The participants’ task is to decide which of the two faces looks, overall,
more feminine. Here the top face is female in the left visual field and the
bottom face is female in the right visual field. From “Perceptual asymme-
tries for free viewing of several types of chimeric stimuli,” by K. E. Luh,
L. M. Rueckert, & J. Levy, 1991, Brain and Cognition, 16, p. 88. Repro-
duced with permission.
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE
member of a pair was counterbalanced, resulting in a matched set of
four pairs of chimeric stimuli from each male/female pair of posers,
yielding a total of 12 stimulus pairs.
Subjects were asked to indicate which of the two faces looked
more feminine overall. The 12 trials were arranged in a random
order determined at run time. As in Experiment 1, participants
indicated their decisions by using both index fingers to press the
response button that spatially corresponded with the selected stim-
ulus. After a response, the display was cleared and a new trial
began after an interstimulus period of 1,500 ms. Again, partici-
pants were requested to examine the stimuli carefully, and were
permitted to respond without time constraints. No feedback was
provided. Three practice trials were administered prior to the
gender chimeric faces test.
Results and Discussion
Responses were categorized according to whether the stimulus
with the salient feature on the left or right side was selected,
irrespective of whether it was the upper or lower. The asymmetry
score for the gender chimeric faces test was calculated by sub-
tracting the number of trials on which the gender decision was
made on the basis of information available on the left side of the
face from the number of trials where the gender decision was made
on the basis of information available on the right side of the face,
and dividing the result by the total number of items (12).
The asymmetry scores for each of the experimental groups are
shown in Figure 5. One-sample t tests again demonstrated that
whereas RPD patients demonstrated a significant left hemispace
bias for gender chimeras, M ⫽ ⫺0.41, SD ⫽ 0.50, t(10) ⫽ ⫺2.73,
p ⫽ .021, r ⫽ .65, both the LPD group, M ⫽ 0.04, SD ⫽ 0.36,
t(8) ⫽ 0.31, p ⫽ .766, and the control participants, M ⫽ ⫺0.22,
0.3
0.2
0.1
0
Asymmetry Score
-0.1
-0.2
-0.3
-0.4
-0.5
-0.6
-0.7
Gender Chimeric Task
Figure 5. Mean asymmetry score on the gender chimeric faces tests for predominantly left-sided Parkinson’s
patients (LPD), predominantly right-sided Parkinson’s patients (RPD), and control participants. Negative scores
indicate a leftward bias for chimeras. Error bars represent the SEM.
451
SD ⫽ 0.47, t(11) ⫽ ⫺1.65, p ⫽ .128, did not. Although a one-way
ANOVA showed no significant main effect of group on asymme-
try scores in the gender chimeric faces test, F(2, 29) ⫽ 2.42, p ⫽
.107, r ⫽ .38, a pairwise comparison between the patient sub-
groups revealed a significant difference between asymmetry
scores, t(18) ⫽ 2.25, p ⫽ .037, r ⫽ .47, suggesting that subgroups
of PD patients, characterized by the side of worse motor symp-
toms, can be differentiated by the degree of lateralized attentional
bias exhibited in a perceptual test which does not involve emotion.
There were no significant differences between asymmetry scores
of the control group and each patient subgroup ( p ⬎ .05).
Of note, correlational analyses performed separately on data
from each subject group revealed that there were no significant
relationships between scores on the gender chimeric faces task and
those obtained in the emotional chimeric faces test administered in
Experiment 1, (LPD: r(9) ⫽ .42, p ⫽ .266; RPD: r(11) ⫽ ⫺.23,
p ⫽ .506; Controls: r(12) ⫽ .25, p ⫽ .434), indicating that the
asymmetries exhibited for the two versions of the chimeric faces
test were independent of each other. There was a highly significant
association between asymmetry scores on the gender chimeric
faces and greyscales in the LPD group, r(9) ⫽ .82, p ⫽ .007,
suggesting some overlap in the underlying processes for making
laterality judgments involved in tasks without an emotional com-
ponent. However, this relationship was not present in either the
RPD group, r(11) ⫽ .29, p ⫽ .396, or controls r(12) ⫽ ⫺.19, p ⫽
.560.
In Experiment 1, right-sided symptoms significantly predicted
performance on both chimeric faces and greyscales tasks (in con-
trast to left-sided symptoms). However, on the gender chimeric
faces test, regression analyses including all PD patients in one
group (with asymmetry score as the dependent variable and right-
LPD
RPD
Control
452 SMITH ET AL.
and left-sided motor symptoms as the independent variables) re-
vealed that neither right-sided symptoms (R2 ⫽ 0.333, ␤ ⫽ ⫺.245,
t(19) ⫽ ⫺1.08, p ⫽ .296) or left-sided symptoms (␤ ⫽ .259,
t(19) ⫽ 1.14, p ⫽ .271) were significantly associated with asym-
metry scores. Of note, there was a significant correlation between
asymmetry score and the ratio of right-to-left motor symptom
severity, r(17) ⫽ ⫺.48, p ⫽ .044, indicating the tendency across
patients for increased bias toward left hemispace as the severity of
right-sided symptoms increased relative to that of left-sided symp-
toms. Correlational analyses revealed no significant associations
with any other clinical or demographic variable, nor with any
measure of basic visual function or neuropsychological test score
( p ⬎ .05).
In summary, the findings from Experiment 2 indicate that the
differences between RPD and LPD patients in laterality judgments
for chimeric stimuli are not necessarily the consequence of differ-
ential patterns of (impaired) emotional processing in subgroups.
Rather, differences in perceptual bias extend to facial chimera
involving decisions regarding gender. It has been argued that
perceptual biases obtained from chimeric studies employing gen-
der are likely to reflect processes that lie closer to true face
processing mechanisms than those employing an emotional judg-
ment (Butler & Harvey, 2008; Gooding, Luh, & Tallent, 2001). In
line with this, Gooding et al. (2001) have shown that medicated
patients with schizophrenia display differential patterns of re-
sponse to emotion and gender chimeras with decreased left atten-
tional bias for the former, concluding that patients with schizo-
phrenia may respond differently to emotion chimeras relative to
healthy controls because of an impaired ability to maintain or
retrieve affective information. While the accuracy of PD patients’
emotional comprehension in Experiment 1 was not specifically
measured, the results here indicate that the strong left hemispace
bias of RPD patients is unlikely to be wholly attributable to
difficulties in comprehending (positive) emotional facial cues.
Rather it appears that lateralized groups of PD patients show
distinct patterns of attentional bias when making laterality judg-
ments of facial stimuli, irrespective of their emotional component.
As before, RPD patients were again the only group to evidence
a significant left hemispace bias, suggesting that damage to striatal
structures that is more extensive on the left side compared to the
right side (with greater disruption to dopaminergic pathways in the
left hemisphere compared to the right) leads to a left-lateralized
perceptual bias for gender chimeras. Yet, although recent literature
indicates that, in general, perception of facial configuration criti-
cally involves the right hemisphere (right fusiform gyrus; Yovel et
al., 2008), and, in particular, that there is a right hemisphere
advantage for the recognition of female faces (Parente & Tom-
masi, 2008), severity of left-sided motor symptoms (indicative of
degree of dopaminergic dysfunction in the right hemisphere) was
not associated with PD patients’ lateralized judgments. Unlike on
emotional chimeric faces, severity of right-sided motor symptoms
(indicative of degree of dopaminergic dysfunction in the left
hemisphere) also failed to predict patients’ asymmetry scores on
the gender chimeric faces task. There was, however, a relationship
between patients’ asymmetry scores and the ratio of right- and
left-sided motor symptom severity. This reflected the tendency for
patients with a larger disparity between severity levels of motor
symptoms on one side of the body and those on the other side to
show more extreme asymmetry scores in the direction contralateral
to the worse-affected side. This suggests that dopaminergic loss in
one hemisphere relative to that in the other is directly related to
both the direction and extent of perceptual bias for gender chime-
ras.
General Discussion
This study examined processing of affective and nonaffective
information in dextral Parkinson’s disease patients with predomi-
nant motor symptoms on the left or right side using chimeric
stimuli. In two experiments, patients with PD predominantly af-
fecting the right side (RPD) showed a larger left hemispace bias
for perceiving chimeric stimuli than did patients with PD predom-
inantly affecting the left side (LPD), although differences were
only significant in the case of the tasks involving decision about
faces and not on greyscales, for which asymmetry scores con-
verged. In Experiment 1 (emotional chimeric faces), differences
between patient subgroups arose from this abnormally large left
hemispace bias in the RPD group. Dopaminergic dysfunction in
the left hemisphere appeared to be strongly associated with a left
hemispace bias for emotional chimeras, as asymmetry scores of
PD patients (irrespective of the side of worse motor symptoms)
correlated significantly with severity of motor symptoms on the
right side of the body. In Experiment 2 (gender chimeric faces), the
only differences to emerge were between a strong left hemispace
bias in RPD and a negligible right hemispace bias in LPD. In this
instance, hemispace bias on the gender task correlated significantly
with the ratio of left-to-right motor symptoms severity of all
patients, indicating that the extent of hemispatial inattention was
related to the degree of hemispheric asymmetry in the dopamine
system caused by PD, on the assumption that the latter is reflected
in the severity of motor impairments. Of note, across all experi-
mental tasks, perceptual bias in patients with PD shared little
association with performance on any of the cognitive tests, con-
sistent with evidence that cognitive task performance in normals is
unrelated to perceptual asymmetry on emotional or nonemotional
tasks of cerebral lateralization (Kim et al., 1990).
The use here of both emotion- and non-emotion-based chimeras
helped to distinguish whether right-handed patients with PD with
asymmetric disease exhibit abnormal perceptual biases only for
emotional stimuli. The fact that differences from controls were
found only for emotional chimeras in RPD is broadly consistent
with the assertion that emotional stimuli are processed differently
from nonemotional stimuli in PD. This is further evidence that
patients with PD have difficulties in recognizing facial emotions,
and that asymmetric hemispheric dysfunction is important in stud-
ies of affective recognition in PD (Clark et al., 2008; Yip et al.,
2003).
Recent meta-analyses of studies performed using PET and fMRI
(Fusar-Poli et al., 2009; Wager, Phan, Liberzon, & Taylor, 2003),
suggest that, contrary to older ideas (Benton, 1990), each hemi-
sphere is specialized for particular types of emotion, the right more
with negative emotions, and the left more with positive emotions
(Fusar-Poli et al., 2009; Root et al., 2006; Wager et al., 2003). In
one study of regional cerebral blood flow, participants with greater
left frontal activation were better at discriminating happy faces
while participants with greater right than left parietal activation
were better at discriminating sad faces (Gur et al., 1994). Since
only happy and neutral expressions were used in the present study,
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE
left hemisphere dysfunction in RPD patients may have produced
an abnormally large left hemispace bias (right hemisphere advan-
tage) in this patient group. To confirm the involvement of emo-
tional processing, one would need to use chimeras of the type used
here, but displaying the variety of negative emotions which have
been reported to be misperceived in PD and may access different
cortical regions from the happy faces in this study (Assogna et al.,
2008; Clark et al., 2008; Yip et al., 2003).
Although the pattern of data in the emotional chimeric faces test
can be explained by the notion of impaired emotion perception in
PD, the finding of a similar pattern in the gender chimeric faces
test cannot. Indeed, PD patients’ perception of gender and familiar
identity from the face appears to remain intact even when their
ability to interpret emotional expressions is compromised (Spren-
gelmeyer et al., 2003). The results of Experiment 2 imply that
asymmetrical dopaminergic dysfunction in PD has a marked effect
on the processing of faces even when there is no emotional
component. It is, of course, well established that biases of visuo-
spatial attention give rise to lateralized performance on both emo-
tion-based facial, non-emotion-based facial, and nonfacial chi-
meric tests (Mattingley et al., 2004, 1994). It seems likely then,
that the large discrepancies in lateralized performance on the
gender chimeric faces test between LPD and RPD patients found
here reflect changes in visuospatial processing. From this view, the
abnormal perceptual bias for emotional chimeras in RPD is likely
to reflect a specific affective processing deficit superimposed on a
more general lateralized deficit of spatial attention.
Areas known to underlie visual attention and spatially guided
behavior, most notably the posterior parietal cortex, are densely
interconnected with basal ganglia structures, including the ventral
putamen and head of the caudate nucleus (Clower et al., 2005;
Middleton & Strick, 2000), both of which are depleted of dopa-
mine even at the earliest stages of PD (Kish, Shannak, & Hornyk-
iewicz, 1988). Asymmetric dopamine depletion in the basal gan-
glia is likely to affect areas receiving inputs from or projecting to
striatal areas, including parieto-temporal areas supporting perfor-
mance on chimeric tests of spatial attention. Yet previous visuo-
spatial research in PD has reported perceptual asymmetries gen-
erally confined to LPD, typically in the form of neglect of left
hemispace, as assessed by measures of perceived size or spatial
extent (Harris et al., 2003; Lee et al., 2001). This is consistent with
studies of patients with unilateral neglect who exhibit a marked
tendency to ignore left visual hemispace, usually associated with
lesions in right hemispheric parieto-temporal and subcortical struc-
tures (Fimm et al., 2001; Karnath et al., 2002; Landis, 2000).
However, ipsilesional biases of spatial attention have also been
observed after both left and right unilateral hemispheric damage,
even in the absence of clinical neglect (Machado & Rafal, 1999;
Mattingley et al., 1994). Similarly, in PD, it is clear that disruption
to either the right- or left-hemispheric dopaminergic system can
lead to neglect-type behavior in the contralateral space. While this
finding appears most obviously in studies of motor neglect
(Bracha, Shults, Glick, & Kleinman, 1987; Milton, Marshall,
Cummings, Baker, & Ridley, 2004), there is emerging evidence
that asymmetric dopaminergic depletion may bias perception and
attention. For example, the perceived midline of PD patients with
left- and right-body side onset deviated from center, in a direction
of which depended on which hemisphere was predominantly af-
fected (LPD: rightward, RPD: leftward). Shifts in opposite direc-
453
tions were also seen in a landmark bisection test in the same study
suggesting a relationship between asymmetric dopaminergic de-
pletion in PD and visuospatial processing, although this effect was
confined to male patients (Davidsdottir et al., 2008). Of note, one
study that included a greyscales task to investigate attentional bias
in Huntington’s disease (HD) reported exaggerated left spatial bias
in symptomatic patients, although this was more pronounced in a
line bisection task than greyscales (Ho et al., 2004). Similarly, a
left hemispace bias was found in HD on a partial-report task,
where subjects reported targets while ignoring distractors (Finke,
Bublak, Dose, Müller, & Schneider, 2006), consistent with the
more pronounced left-hemispheric neuropathology in Hunting-
ton’s disease (Muhlau et al., 2007).
The present results then, consistent with those of Finke and
colleagues (2006), point to the leftward lateralization of aspects of
spatial attention in patients who are likely to have depleted levels
of dopamine in the left striatum. Moreover, patients’ performance
on the gender chimeric faces extend these findings, indicating that,
at least in tasks involving some kind of competition between the
hemispheres such as chimeric faces, the nature of the changes may
crucially depend on which hemisphere of the brain is more af-
fected and the degree of asymmetry present, as well as on the
nature of the task (Foster, Black, Antenor-Dorsey, Perlmutter, &
Hershey, 2008). PD patients’ lateralized spatial bias for gender
chimeras reflects a greater attentional weighting of the least af-
fected hemifield at the expense of the most affected hemifield,
rather than complete unawareness, as in pure neglect (Desimone &
Duncan, 1995; Finke et al., 2006). In line with the view that striatal
components within (lateralized) cortico-subcortical brain circuits
serve the same function as the cortical regions with which they
communicate (Middleton & Strick, 2000), recent work has uncov-
ered deficits in visuospatial cognition in PD patients with right-
and left-body side of motor symptom onset that closely resemble
that of patients with left and right posterior parietal damage,
respectively (Amick et al., 2006; Schendan et al., 2008).
The lack of neglect-type behavior in the present LPD group
contrasts with that found in previous studies which report a mild
right-hemispace perceptual bias (Davidsdottir et al., 2008; Ebers-
bach et al., 1996; Lee et al., 2001). However, this may be a
reflection of the (insignificantly) reduced motor (and so likely
striatal dopamine depletion) asymmetry in our LPD group. Al-
though we have shown the importance of assessing asymmetry, it
was not assessed in the first two of the above studies who report
only side of disease onset or side of worse symptoms.
Both emotional and gender chimeras differentiated the LPD and
RPD groups, but greyscales did not. Although this may reflect
greater sensitivity of facial chimeric tests, it is not clear whether
this reflects a face-specific anomaly rather than a more general
disturbance of attention. Consistent with earlier work showing that
there may be distinct lateralized mechanisms which produce dif-
ferent patterns of attentional bias for different stimuli (Gooding et
al., 2001; Luh et al., 1991; Mattingley et al., 1994; Nicholls et al.,
1999), except for a strong association in laterality judgments
between gender chimeric faces and greyscales and a moderate
association between emotional chimeric faces and greyscales in
LPD, intertask associations tended to be small and nonsignificant.
In contrast to previous findings in healthy right-handers of left
hemispace biases that are greater for face than nonface stimuli, and
are greater still when the face task has an emotional component.
454 SMITH ET AL.
(Gooding et al., 2001; Luh et al., 1991), our controls exhibited the
reverse pattern, that is, the largest left hemispace bias for grey-
scales and the smallest for emotional chimeric faces. This may
reflect the mediation of left hemispheric structures in the process-
ing of happy faces, but might also be due to the increased com-
plexity of the emotional chimeric faces, and the participants’ age.
There is evidence that bihemispheric structures are recruited in
older adults (so reducing the left hemispace bias to nonsignificant
levels) as visuospatial task difficulty increases (Butler & Harvey,
2008; Failla, Sheppard, & Bradshaw, 2003). This would not be
possible in our RPD group, because putative dopamine depletion
the left striatum would not allow equal recruitment in both hemi-
spheres. In any case, the contrast between patterns of spatial bias
across chimeric tasks of varying complexity in PD and control
participants is striking, especially given their comparable age and
similar cognitive status.
There were several limitations in the present study. First,
though widely used in investigations of cerebral asymmetries
(e.g., Failla et al., 2003; Levy et al., 1983; Luh et al., 1991;
Rueckert, 2005; Rueckert & Naybar, 2008), our facial stimuli
(spliced not blended photographs) do not necessarily engage
normal mechanisms of face perception (Butler & Harvey,
2008), though there is presumably substantial overlap. Second,
directional eye movements can enhance lateral perceptual bias
(Butler et al., 2005; Butler & Harvey, 2008; Chokron, Bartolo-
meo, Perenin, Helft, & Imbert, 1998). Fixations and saccades
were not recorded in the present study, so we cannot directly
evaluate their role in laterality judgments, particularly the large
left hemispace bias exhibited by RPD patients. Although eye
movements in PD may be restricted in certain directions, most
commonly for upward gazing (Corin, Elizan, & Bender, 1972),
this typically occurs when the task is to gaze on command
rather than when required to gaze at a target (as in the clinical
examination and, in effect, the experimental tasks used here),
which may be why so few of the patients showed any such
restrictions. In addition, basal ganglia dysfunction can lead to
hypometric saccades (Winograd-Gurvich et al., 2003), and three
patients in this study evidenced slight hypometria on clinical
examination that was more evident toward targets in left hemis-
pace. Yet two of these patients, who had RPD, displayed strong
left-lateralized bias in perceptual measures while the other
patient, who had LPD, exhibited small right-lateralized bias
across tasks, suggesting asymmetrical dysfunction of the basal
ganglia and related circuitry was more important than oculo-
motor deficits in determining direction and extent of observed
attentional bias.
The male-to-female ratio was somewhat different in the RPD
group (predominantly male) compared to the LPD and control
groups (approximately equal numbers of males and females), and
there is evidence on visuospatial tasks that males tend to be more
right hemisphere lateralized (Jewell & McCourt, 2000). Yet most
chimeric studies have reported that, irrespective of gender, partic-
ipants tend to attend more to the left-side of chimeric faces (Levy
et al., 1983; Luh et al., 1991; Rueckert, 2005). Further, a recent
study reported no significant differences between males and fe-
males using the Levy version of the chimeric faces task (as used in
the present study), with females evidencing a numerically larger
left hemispace bias (Rueckert & Naybar, 2008). Nevertheless,
specific gender differences in PD have been reported in both
self-reports of visuospatial problems (Davidsdottir, Cronin-
Golomb, & Lee, 2005) and visuospatial tasks (Davisdottir et al.,
2008), so that in a line bisection task men in the RPD group
deviated toward the left, whereas women were close to the mid-
point. In contrast, LPD men displayed a small rightward deviation
and women a similar left deviation. However, in the present study,
the discrepancy in gender ratios between patient subgroups (and
controls) failed to account for the groups’ contrasting patterns of
perceptual asymmetry on chimeric faces tasks, and right-sided
symptoms predicted patients’ perceptual bias for emotional chi-
meras even after controlling for gender.
Tests using chimeric stimuli offer a new approach to investigate
deficits in emotional processing and spatial attention in patients
with asymmetric PD, showing that LPD and RPD patients process
the left and right regions of faces differently. The results from both
experiments strongly suggest that the degree of asymmetry in
dopaminergic degeneration in each hemisphere is related to later-
alization of visuospatial attention in Parkinson’s disease, although
emotional processing may also be affected. There are likely to be
important applications for this research. As previously noted, in
studies with healthy participants, left-lateralized performance in
emotional chimeric faces has been shown to significantly correlate
with scores on measures of emotional awareness and empathy,
suggesting that as right hemisphere dominance in the perception of
facial emotion increases, the ability to perceive complexity during
the processing of emotional information increases (Lane, Kivley,
Du Bois, Shamasundara, & Schwartz, 1995; Rueckert & Naybar,
2008; Rueckert & Pawlak, 2000). Further studies are needed to
elucidate the functional significance of an abnormally large left
spatial bias for emotional chimeras, as displayed by patients with
predominantly right-sided symptoms, and how this links with
impaired emotional processing.
Visuospatial asymmetries are also likely to have practical sig-
nificance for navigation in PD. Leftward attentional bias in healthy
people causes a subtle rightward neglect, which results in more
rightward collisions (Nicholls, Loftus, Mayer, & Mattingley, 2007;
Nicholls, Loftus, Orr, & Barre, 2008). Veering in Parkinson’s
patients also appears to correspond to the shifting of the perceived
midline, with LPD patients evidencing a rightward shift in veering
whereas RPD patients (like healthy controls) veer leftward (Dav-
idsdottir et al., 2008). Further, in healthy controls, levadopa im-
proves straight-line walking (by reducing veering), indicative of a
link between asymmetric organization of dopaminergic function
and the spatial orientation skills involved in navigation (Mohr,
Landis, Bracha, Fathi, & Brugger, 2003). In HD, asymmetry
indices on greyscales were significantly related to visual perfor-
mance during driving (Tant, Brouwer, Cornelissen, & Kooijman,
2002). Therefore, patterns of attentional bias in PD, illustrated
most clearly in this study by the exaggerated left hemispace bias of
RPD patients, have the potential to affect patients’ everyday in-
teractions with the environment. Impaired spatial navigation dur-
ing gait is well known in Parkinson’s disease (Davidsdottir et al.,
2005, 2008; Lee & Harris, 1999), as are problems with driving (Uc
et al., 2007). With this in mind, research intended to investigate the
relationship between these difficulties and attentional bias in PD
participants, perhaps with a focus on the influence of dopaminergic
medication, is likely to be beneficial in understanding the precise
nature of patients’ problems with navigation in everyday settings
and how they may best overcome them.
 PERCEPTUAL BIAS IN ASYMMETRIC PARKINSON’S DISEASE
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Received August 20, 2009
Revision received November 24, 2009
Accepted November 25, 2009 䡲