Cognitive Brain Research 25 (2005) 78 – 89
www.elsevier.com/locate/cogbrainres
Research Report
Summation of semantic priming and complex sentence comprehension
in Parkinson’s disease
Anthony J. Angwina,*, Helen J. Chenerya, David A. Coplanda,
Bruce E. Murdocha, Peter A. Silburna,b
a
Centre for Research in Language Processing and Linguistics, Division of Speech Pathology, The University of Queensland, Brisbane 4072, Australia
b
Department of Neurosciences, Princess Alexandra Hospital, Brisbane, Australia
Accepted 13 April 2005
Available online 13 May 2005
Abstract
Research has suggested that the integrity of semantic processing may be compromised in Parkinson’s disease (PD), which may account
for difficulties in complex sentence comprehension. In order to investigate the time course and integrity of semantic activation in PD, 20
patients with PD and 23 healthy controls performed a lexical decision task based on the multi-priming paradigm. Semantic priming effects
were measured across stimulus onset asynchronies of 250 ms, 600 ms, and 1200 ms. Further, PD participants performed an auditory
comprehension task. The results revealed significantly different patterns of semantic priming for the PD group at the 250-ms and 1200-ms
SOAs. In addition, a delayed time course of semantic activation was evident for PD patients with poor comprehension of complex sentences.
These results provide further support to suggest that both automatic and controlled aspects of semantic activation may be compromised in
PD. Furthermore, the results also suggest that some sentence comprehension deficits in PD may be related to a reduction in information
processing speed.
D 2005 Elsevier B.V. All rights reserved.
Theme: Disorders of the nervous system
Topic: Degenerative disease: Parkinson’s
Keywords: Levodopa; Parkinson’s disease; Semantic priming; Sentence processing; Signal-to-noise ratio
1. Introduction
Parkinson’s disease (PD) is a progressive neurological
condition, associated with striatal dopamine depletion.
Although PD is primarily characterized by movement
disorders, a variety of cognitive deficits and subtle language
deficits are also a frequently reported feature. While the
potential role of dopamine as an important neuroregulator of
cognitive functioning has been recognized [46], disruption to
the functioning of the striatum and the dopamine dependent
connections to the frontal lobes may also be expected to
influence cognitive functioning. Consistent with this theory,
* Corresponding author. Fax: +61 7 3365 1877.
E-mail address: [email protected] (A.J. Angwin).
0926-6410/$ - see front matter D 2005 Elsevier B.V. All rights reserved.
doi:10.1016/j.cogbrainres.2005.04.008
it has been suggested that the cognitive deficits in PD may be
consistent with a disturbance to frontal – striatal function [8].
Accordingly, given the role of dopamine and the striatum on
cognitive function, it is not unexpected that language
function may also be impaired. Indeed, researchers have
illustrated that the integrity of semantic processing may be
compromised in PD [7,48].
Recently, the use of various online semantic priming tasks
has been central to the investigation of semantic processing.
During a semantic priming task, lexical decisions to Ftarget_
words are typically faster if they are preceded by a semantically related Fprime_ word (e.g., tiger– stripes). A generally
accepted theory postulates that during a semantic priming
task, the presentation of the prime causes an automatic
spreading of activation, which partially activates other related
concepts, thereby speeding lexical decisions to semantically
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
related target words [16]. Thus, by manipulating the stimulus
onset asynchrony (SOA) (i.e., the time lapse between
presentation of the prime and target), the time course over
which automatic semantic activation occurs can be estimated.
It is also important to note that attentional or controlled
processes can induce semantic priming effects, but these
processes typically emerge when longer SOAs are used and
when the proportion of related word pairs is high [45].
Certainly, disruptions to fast acting/automatic as opposed to
controlled semantic processing may be most expected in PD,
as it is proposed that dopamine and the striatum have a
substantial influence on the integrity and speed of information processing.
Servan-Shreiber et al. [50] have proposed that the
function of dopaminergic modulating systems is to dampen
weak signals (noise) while at the same time amplifying
stronger signals (excitatory or inhibitory) in neural areas.
Furthermore, Cepeda and Levine [12] suggested that
dopamine is able to increase the signal-to-noise ratio in
the neostriatum by integrating relevant information and
screening out less relevant information. It could be expected
from this research, therefore, that changes to dopaminergic
functioning will change the signal-to-noise ratio of information processing and subsequently influence language
function.
This argument is supported by semantic priming
research, which has suggested that dopamine may have a
neuromodulatory influence on semantic processing. For
example, Kischka et al. [33] examined the influence of
dopamine on semantic activation by administering levodopa
to healthy young adults. The results led the researchers to
suggest that dopamine may modulate automatic semantic
activation, by increasing the signal-to-noise ratio in semantic networks. Similar research by Angwin et al. [3] also
aimed to examine the influence of dopamine on the time
course of semantic activation. The results revealed an earlier
onset and decay of semantic activation in participants who
had ingested levodopa, as measured by tests of direct (e.g.,
tiger – stripes) and indirect (e.g., lion – stripes) priming.
Thus, Angwin et al. [3] suggested that dopamine may
influence the time course of semantic processing.
Similarly, researchers have also suggested that the
striatum is a key area of the brain that may support
information processing speed [28,47,49]. Thus, there is
converging evidence to suggest that both dopamine and the
striatum influence the speed of information processing,
which may subsequently affect language function. Given
the striatal dopamine deficiency in PD, delays in semantic
activation may be expected to occur in this population.
Reports on the integrity of semantic activation in PD,
however, have been inconsistent. Specifically, while the
results of some research has suggested that semantic
activation may be intact in PD [19,29,52], the results of
other research has illustrated a delayed time course of
semantic activation in patients with the disease [4]. In
addition, researchers have also suggested that the integrity
79
of controlled or attention-based semantic processing at
longer SOAs may be compromised in PD [4,18]. Such
variability in the literature has consequently sparked debate
as to whether the integrity of semantic activation in PD is
compromised or not. Accordingly, further research that aims
to chart the integrity and time course of semantic activation
in PD is both timely and important.
The use of a multi-priming paradigm, as implemented by
Balota and Paul [5], may be particularly useful for charting
the time course and integrity of semantic activation. The
multi-priming paradigm differs from standard semantic
priming tasks, by implementing multiple prime words.
Specifically, two prime words can be presented, with either
the first, second, or both prime words semantically related to
the target word. Consequently, while standard priming
effects can be measured from one related prime that directly
precedes the target (e.g., soup –stripe – TIGER), semantic
priming effects can also be measured when only the first
prime or both prime words are related to the target.
Therefore, the measurement of semantic activation across
conditions that are not available in traditional single prime
lexical decision tasks may provide further information about
the integrity of semantic activation in both PD and healthy
adults.
Analysis of semantic priming when only the first prime
word is related to the target (e.g., lion –buckle –TIGER)
allows researchers to assess both the strength and persistence of semantic activation across an intervening word. For
instance, while Balota and Paul [5] did find priming across
an intervening unrelated word in healthy adults using
associatively related word pairs, the magnitude of this
priming effect was smaller than the priming effect obtained
when no intervening unrelated word was presented prior to
the target. The further use of a multi-priming paradigm, may
clarify whether semantic priming is in fact sensitive to
disruption across an unrelated word, and whether this
phenomenon is exaggerated in PD due to dopamine
depletion or deficient information processing. In addition,
by presenting two prime words that are unrelated to each
other, but converge onto the same semantic representation
(e.g., lion –stripes –TIGER), it is possible to assess whether
a summation of activation occurs. Balota and Paul [5]
demonstrated a summation of activation, such that the use of
two related prime words yielded larger priming effects than
the single related prime conditions. Hence, such comparisons may provide further insight into the integrity and
strength of spreading activation during semantic processing
in PD.
To date, while the multi-priming paradigm has been used
by researchers to investigate aspects of semantic processing
and summation of activation in aphasic patients [13,40,41]
and people with schizophrenia [14], the use of this paradigm
in the PD population remains a mostly unexplored avenue
of research. Recently, we used a multi-priming paradigm to
investigate the integrity of automatic semantic activation in
PD patients and healthy older adults at a short 250 ms SOA
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A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
[2]. While no summation priming was observed for either
group, the control group demonstrated significant semantic
priming effects for all prime conditions. For the PD group,
however, semantic priming effects were evident when the
second prime or both prime words were related to the target,
but not when only the first prime was related to the target.
Consequently, we suggested that the results were consistent
with a reduction in the signal-to-noise ratio of information
processing in PD. More specifically, we suggested that due
to a reduction in the salience of a related prime word (i.e.,
the signal), or an increase in the salience of an unrelated
prime word (i.e., the noise), then semantic priming effects
may be disrupted when an unrelated word is presented
between the related prime and the target.
Research also suggests, however, that the ability to direct
attention during semantic processing may be impaired in PD.
Copland [17] has suggested that basal ganglia dysfunction
may interrupt attention-based selective engagement of the
semantic network. Moreover, it has been shown that PD
patients experience difficulties in semantic set shifting on a
lexical decision task [38], which may also be consistent with
PD patients’ difficulties focusing on salient information and
ignoring irrelevant information [37]. Similarly, such difficulties may also extend to automatic semantic processing in
PD, such that spreading activation cannot be constrained to
the related prime word when an unrelated word directly
precedes the target. More specifically, the inability to inhibit
the influence of the intervening unrelated word in PD may
disrupt semantic activation. Indeed, Gurd and Oliveira [26]
revealed that PD patients experienced difficulties selecting
an appropriate word in the presence of semantic competitors
in a word search task, which suggests that semantic
inhibitory processes may be impaired. Hence, a reduced
signal-to-noise ratio and reduced semantic inhibition both
have the capacity to explain disruptions to semantic priming
across an intervening unrelated word.
One unexpected outcome of Angwin et al.’s [2] research,
however, was that the absence of priming effects across an
unrelated word occurred in PD despite significant semantic
priming effects for the other related prime conditions.
Significant priming effects at a short SOA suggested a
normal speed of semantic activation in PD. Thus, the results
were inconsistent with previous research that has suggested
a delayed time course of semantic activation in PD.
Research by Grossman et al. [24], however, has begun to
elucidate the potential reasons for such variable findings,
suggesting that delayed semantic activation in PD may be
linked to poor comprehension of complex sentences, which
is only evident in some patients with the disease.
It has long been recognized that some patients with PD
may present with deficits in processing complex sentences
[20,32,39,43]. In particular, their comprehension difficulties
are often evident for sentences with a noncanonical structure
such as object relative (OR) sentences (e.g., the boy that the
girl chased was fast), as opposed to those with a canonical
structure such as subject relative (SR) sentences (e.g., the boy
that chased the girl was fast) [22,42]. More importantly,
Grossman et al. [24] recently demonstrated that a subgroup of
PD patients presented with poor comprehension of OR
sentences also presented with a delayed time course of
semantic activation, as evidenced by semantic priming
effects only at an abnormally long inter-stimulus interval
(ISI). In contrast, the time course of semantic activation
appeared to be intact for a subgroup of PD patients with intact
comprehension of OR sentences. Such links between speed
of semantic activation and complex sentence comprehension
are not unexpected, given the additional processing requirements associated with processing noncanonical sentences.
In order to comprehend an OR sentence such as the girl i
that the boy chased (t i ) was fast, the first noun phrase (NP)
the girl must be understood to be the object of the verb (V)
chased, despite the fact that it occurs at the beginning of the
sentence. A generally accepted theory is that the movement
of the NP leaves a phonologically empty NP or placeholder
at the position of the gap, referred to as a trace (indicated by
the subscript (t i ) in the example) [15]. During the online
processing of such a sentence, the antecedent (indicated by
the subscript i in the example) must be reactivated at the
position of the gap, thereby allowing thematic roles to be
assigned. Sentence comprehension may be compromised,
therefore, if the antecedent is not rapidly reactivated. As a
result, a sufficient speed of information processing is
required in order for trace reactivation to occur, and
measures of semantic activation may be an effective
indicator of information processing speed in PD.
Accordingly, only those PD patients with poor comprehension of noncanonical sentences may be expected to
present with a delayed time course of semantic activation. In
contrast, however, the results of our previous research [2]
indicate that the presence of an intervening unrelated word
can disrupt semantic processing in PD independently of any
change to the time course of semantic activation. Thus,
disruption of semantic priming effects across an intervening
word may be expected even in those PD patients with good
comprehension of noncanonical sentences, since trace
reactivation should remain unaffected.
The aims of the present research were based upon
evidence, which suggests that the integrity of automatic
semantic activation in PD may be compromised. Specifically, this research aimed to chart the time course of semantic
activation in PD patients and healthy control participants
using a multi-priming paradigm and multiple SOAs (the
authors recognize that priming effects observed at longer
SOAs may reflect the influence of some controlled processing). Furthermore, this research also aimed to examine the
influence of semantic activation on comprehension of
noncanonical sentences in PD. The following predictions
were made: (a) that the control group will demonstrate
significant priming effects for each prime condition at each
SOA; (b) that the integrity of semantic activation will be
disrupted in PD, as indicated by an absence of priming
effects across an intervening unrelated prime word at each
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
81
SOA; and (c) that a correlation will be observed between the
time course of semantic priming and the comprehension of
noncanonical sentences in PD. In particular, we predict that a
subgroup of PD patients with good comprehension of
noncanonical sentences will demonstrate significant priming
effects at 250 ms SOA when the second prime word or both
prime words are related to the target. In contrast, we predict
priming effects will be absent for each prime condition at
250 ms SOA for a subgroup of PD patients with poor
comprehension of noncanonical sentences.
levodopa, average daily dosage was 606.94 mg (SD 360.33;
range 100– 1500), while for participants taking Cabaser,
average daily dosage was 2.0 mg (SD 1.55; range 1.0– 4.0).
In addition to their dopaminergic supplementation, one of the
PD participants was taking Amantadine (Symmetrel), two
were taking trihexyphenidyl (Artane), and one was taking
pergolide (Permax). Care was taken to ensure that PD
participants were achieving maximum clinical benefit from
their medication at the time of testing. Therefore, testing of
the PD group was conducted approximately 45 min after
dosage.
2. Methods
2.2. Semantic priming task stimuli
2.1. Participants
The experiment was a 2 3 4 (Group SOA Prime) mixed factor design, with group as a betweensubjects factor and SOA and prime as within-subject factors.
Experimental stimuli consisted of 12 critical word triplets,
the first two words being the primes (P1 and P2), and the
third, the target. Prime stimuli always consisted of real
English words; however, target stimuli consisted of both real
English words and pronounceable nonwords. For each
critical word triplet a prime word was either related or
unrelated to the target, resulting in four prime conditions;
related– related (RR), related – unrelated (RU), unrelated –
related (UR), and unrelated – unrelated (UU). The UU prime
condition was used to calculate priming effects in each of
the three related prime conditions. With four prime
conditions per critical word triplet, a total of 48 critical
trials were created. An example of a critical trial and the four
prime conditions was as follows:
Twenty participants with idiopathic PD (confirmed by a
neurologist using Calne et al.’s [9] criteria for diagnosing
PD) and 23 non-neurologically impaired control participants
comprised the study’s two subject groups. All participants
were right-handed, native speakers of English with no
history of neurological surgery, drug or alcohol abuse, or
dementia. The Dementia Rating Scale 2 (DRS-2) [31] was
used to assess the cognitive status of all participants prior to
the commencement of testing. DRS-2 scores were significantly lower for the PD group (t(41) = 5.99, P < 0.001);
however, all scores were above the recommended lower
boundary for normal performance. The two groups did not
differ with respect to sex distribution, age or education.
Table 1 provides a summary of group demographics.
Experiments were conducted with the understanding and
written consent of each participant.
The PD group had a mean disease duration of 4.8 years
(SD 3.04; range 1 –12) and a mean age at onset of 59.55
years (SD 5.58; range 52 –72). Hoehn and Yahr scores [30]
were used to classify the disease severity of the PD
participants, with a mean score of 2.08 (SD 0.57; range
1 –3). Predominant symptoms were tremor for 16 participants and bradykinesia/rigidity for four participants. In
addition, symptoms were predominantly left sided for six,
right sided for five and bilateral for nine participants.
Eighteen of the patients in the PD group were receiving
dopaminergic therapy in the form of levodopa (Madopar/
Sinemet), seven patients were taking Cabaser, and one patient
was not receiving any medication. For participants taking
Table 1
Demographics for the PD and control groups
Group
Male – Female
Age
Education
DRS-2
PD
Control
13:7
64.30 (4.75)
11.50 (2.70)
139.25 (2.09)
12:11
63.22 (6.03)
13.00 (2.82)
142.48 (1.41)
Standard deviations in parentheses.
Abbreviations: PD, Parkinson’s disease; DRS-2, Dementia Rating Scale-2.
(RR) summer – snow –winter
(RU) summer – hill – winter
(UR) island– snow – winter
(UU) island – hill –winter
The majority of words used were nouns; however, some
verbs, adverbs, and adjectives were also incorporated into
the stimuli. The critical target words and their related primes
were derived from the Edinburgh Associative Thesaurus
(EAT) [34], such that the probability that a target word would
be produced as an associate to the prime word was high.
Furthermore, care was taken to ensure that all related prime
words shared an obvious semantic relationship with the
target word (e.g., judge –jury). Unrelated prime words were
matched in length and frequency [35] to the related prime
words already serving as stimuli in the experiment. Both
related and unrelated prime words in each condition were
always unrelated to each other according to the EAT [34].
In order to lower the relatedness proportion (RP) of the
experiment, and thereby reduce the potentially confounding
effects of post-lexical strategy use, an additional 12 filler
targets were created. These filler target words were matched
to the length and frequency [35] of the target words used in
the critical trials. Additionally, for each of these fillers, four
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A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
prime words were constructed. Two of these prime words
were matched to the length and frequency [35] of P1 in the
critical trials, and two were matched using the same criteria to
P2 of the critical trials. Consequently, each filler target could
be repeated four times, each with a different prime (i.e., P1/
P2) combination, in the same manner as the critical trials. The
resulting total of 48 filler trials, involving repeated presentation of the same target words, was intended to reduce the
salience of the repeated critical trial presentations. All prime
words used in the filler trials were both unrelated to each
other and unrelated to the target. The resulting RP of the
experiment following the addition of these filler trials was
0.38.
In addition to the 96 word target trials, a further 12
pronounceable nonword targets were created. All nonwords
were derived by changing one to three phonemes in existing
English words (not already serving as stimulus items in the
experiment), which were matched in length and frequency
[35] to the critical word targets used in the experiment. For
each of the 12 nonword targets, four different prime words
were created, using the same criteria as that used for the
construction of the filler trials. The nonword ratio (defined as
the number of word prime/nonword targets divided by the
number of word prime/unrelated word targets plus word
prime/nonword targets) was 0.44 and the probability of a
nonword was 0.38.
A total of three separate stimulus lists were constructed
for the present experiment, one for each SOA. Each list
consisted of 48 critical targets, 48 filler targets, and 48
nonword targets, resulting in a total of 144 trials for each
stimulus list. The order of stimulus items in each list was
initially pseudorandomized and then held constant for all
presentations of that list to all participants. In order to avoid
presenting the four prime conditions for each critical word
triplet (i.e., RR, RU, UR, UU) in the same order, care was
taken to counterbalance the order of presentation within
each list. Consistent with Hagoort [27], counterbalancing
was achieved by taking a different random sample of 12
from the 24 possible orders of presentation, for each of the
three experiments. These 12 orders were then assigned
randomly to the 12 critical word triplets for each experimental list. Furthermore, repeated critical target words were
separated by a minimum of 20 trials within each list. In this
way, the potentially confounding influence of repeated
exposure to the same target stimuli could be minimized.
Nonetheless, it is possible that RTs may still be influenced
by the repeated nature of the critical targets. For the
purposes of statistical analyses, therefore, the position of
each target in the list (i.e., first, second, third, or fourth
presentation) was recorded. This position was then used as a
covariate during analyses, to account for any influence
repetition may have on RTs.
All participants received the three lexical decision
experiments in the same order (i.e., 250 ms SOA, then
600 ms SOA, then 1200 ms SOA). These three experiments
were completed during different testing sessions held at
least 2 weeks apart, in order to reduce the influence of
repeated exposure to the same stimuli across the three
experiments. All stimuli were presented on a portable laptop
computer using Superlab experimental software (Version
2.0) [11], which measured participants’ RTs via a Cedrus
response pad (model RB-420) (accurate to within 1 millisecond) and collected all error and RT data automatically.
Button 2 on the response pad was labeled FYes_ and button 3
on the response pad was labeled FNo_.
2.3. Procedure
Participants were informed that two consecutive words,
which they may or may not recognize, would appear very
quickly in the center of the screen. These words would then
be followed by a third word, which would appear in the
same position. They were asked to make a lexical decision
to the third word as quickly and as accurately as possible, by
pressing the Fyes_ button if it was a real word or the Fno_
button if it was a nonword. A set of 12 practice trials,
featuring the same SOA as the experiment that followed,
was given to each participant prior to testing.
All stimuli were presented in 70-point Arial font, in the
center of the computer screen. Prime words were presented
in lower case letters while the target word appeared in
uppercase letters. The sequence of events for both practice
and experimental trials was as follows: (a) a fixation point
appeared in the center of the screen for 500 ms; (b) after a
blank screen interval of 200 ms, the first prime word was
displayed for 100 ms; (c) a blank screen was then presented
followed immediately by the second prime for 100 ms; (d) a
blank screen was then displayed again followed immediately by the target word, which was displayed for 3000 ms
or until the participant responded by depressing a button;
and (e) the next trial was then activated automatically, 1200
ms after the previous target disappeared from the screen.
The blank screen intervals between P1 and P2, and P2 and
the target were either 25 ms (SOA 1), 200 ms (SOA 2), or
500 ms (SOA 3). Hence, the total SOA for each list was 250
ms, 600 ms, or 1200 ms. Fig. 1 illustrates the procedure
used for a typical trial (from P1 to target). Experimental
stimuli were presented to participants via three blocks of 48
trials, with a short rest break between each block. Additionally, five buffer trials were included at the beginning of
each block to allow participants to become comfortable with
the experiment, before the timed trials began.
2.4. Auditory comprehension task stimuli
Experimental sentence stimuli were administered as part
of a larger comprehension test battery, divided into two
stimulus sets. The order of presentation of all sentences was
randomized, and then held constant for each participant,
with each stimulus set administered during a separate testing
session. The experimental stimuli of interest to the present
study were 12 SR sentences (e.g., the boy that liked the girl
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
83
Fig. 1. An illustration of the procedure used for a typical trial (from P1 to target) during the lexical decision task.
bought an ice cream) and 12 OR sentences (e.g., the child
that the mother kissed heard the noise). All sentences were
plausible in both forward and reverse directions, to ensure
that participants could not use the plausibility of thematic
roles to guide their answers.
For each sentence, a question was designed that probed
understanding of the thematic roles associated with each
sentence. For both SR and OR sentences, four questions
probed the subject of the first verb, four questions probed
the object of the first verb, and four questions probed the
subject of the main verb. Therefore, for the sentence Fthe
child that the mother kissed heard the noise_, the possible
comprehension probes would be as follows: (a) who was
kissed, (b) who did the kissing, or (c) who heard the noise.
2.5. Procedure
Participants were instructed to listen to each sentence and
answer the question that followed the sentence as accurately
as possible. The researcher read each sentence at a standard
speaking rate, followed immediately by the question.
Repetitions of the question were allowed; however, no
repetition of the sentences was given to participants.
Participants’ answers were recorded verbatim at the time
of testing. All participants were provided with practice
sentences, prior to conducting the experiment proper.
3. Results
3.1. PD group versus control group
Only RTs for the critical trials were analyzed. All
participant errors and all RTs less than 200 ms or greater
than 1500 ms were removed from analyses, resulting in the
removal of 2.04% of the PD group’s and 1.08% of the
control group’s data. Due to the low percentage of errors, no
analyses were conducted on the error data. Outliers were
treated by calculating Tukey’s biweight mean estimators for
each participant and condition, and replacing any RTs more
than two standard deviations above or below the mean with
the appropriate mean estimator. This resulted in the
replacement of 4.32% of the PD group’s data and 4.11%
of the control group’s data. Tukey’s biweight mean
estimators were then calculated for each group and
condition, resulting in the replacement of a further 7.26%
of the PD group’s data and 4.11% of the control group’s
data.
Table 2 displays the mean RTs (covaried for position of
target presentation) for both the PD and control groups as a
function of SOA and prime. Individual participant RTs were
entered into a mixed linear model analysis with subject as a
random factor, group (PD, control) as a between-subjects
factor, SOA (250 ms, 600 ms, 1200 ms), and prime (RR,
RU, UR, UU) as within-subject factors and position as a
covariate. The results revealed significant main effects of
SOA and prime [ F(2,6036) = 111.27, P < 0.001; and
F(3,6036) = 20.76, P < 0.001, respectively] and significant
interaction effects of Group SOA and SOA Prime
[ F(2,6036) = 27.74, P < 0.001; and F(6,6036) = 6.04, P <
0.001, respectively], with a main covariate effect of position
[ F(1,6036) = 106.89, P < 0.001].
While the main and interaction effects are provided for
descriptive purposes, the data provided therein do not test
explicitly whether there was a differential pattern of priming
across time between the two groups. Consequently, of
particular interest in this experiment were the priming
effects for each prime condition and SOA. Priming effects
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A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
Table 2
Mean RTs for the PD and control groups as a function of SOA and prime condition
Prime condition
Group
Control (n = 23)
PD (n = 20)
SOA
SOA
250
Related – related
Related – unrelated
Unrelated – related
Unrelated – unrelated
629
651
626
671
600
(103)
(115)
(109)
(123)
601
598
589
613
(98)
(85)
(85)
(98)
1200
250
594
600
598
613
627
644
623
651
(85)
(88)
(81)
(108)
600
(119)
(121)
(122)
(122)
608
594
588
617
1200
(122)
(88)
(96)
(118)
624
629
639
632
(110)
(116)
(130)
(113)
RTs reported in milliseconds; standard deviations in parentheses.
Abbreviations: PD, Parkinson’s disease; SOA, stimulus onset asynchrony.
were analyzed separately for each group and SOA, therefore, by way of planned pairwise comparisons between the
related prime conditions (RR, RU, UR) and the UU
condition. These comparisons were conducted after adjusting for the significant position effect.
Analysis of the control group’s data revealed significant
priming for RR, RU, and UR priming conditions at the 250ms SOA [t(6036) = 5.84, P < 0.001; t(6036) = 2.74, P =
0.006; and t(6036) = 6.22, P < 0.001, respectively]. In
contrast, only significant RU and UR priming effects were
evident at 600 ms SOA [t(6036) = 2.1, P = 0.035; and
t(6036) = 3.32, P = 0.001, respectively], while significant
RR and UR priming effects were evident at the 1200-ms
SOA [t(6036) = 2.66, P = 0.008; and t(6036) = 2.06, P =
0.04, respectively]. Analysis of the PD group’s data revealed
significant priming for the RR and UR conditions at 250 ms
SOA [t(6036) = 3.09, P = 0.002; and t(6036) = 3.65, P <
0.001, respectively], and significant priming for the RU and
UR conditions at 600 ms SOA [t(6036) = 2.97, P = 0.003;
and t(6036) = 3.69, P < 0.001, respectively]. In contrast,
no significant priming effects were evident at the 1200-ms
SOA.
While the analyses reported thus far provide an
indication of which priming effects were significant for
each group and SOA, they fail to establish whether the
magnitude of priming differed for any of the related prime
conditions. More importantly, they also fail to establish
whether a summation of priming occurred for either group at
each SOA (i.e., whether the magnitude of priming for the
RR condition was larger than that of the RU and UR
conditions). Hence, further planned pairwise comparisons
were conducted among the three related prime conditions.
Analysis of the control group’s data revealed that RTs to
both the RR and UR conditions were significantly faster
than the RTs to the RU condition at 250 ms SOA [t(6036) =
3.11, P = 0.002; and t(6036) = 3.50, P < 0.001,
respectively]. No other comparisons were significant.
Similarly, analysis of the PD group’s data also revealed
that RTs for the RR and UR conditions were faster than the
RTs for the RU condition at 250 ms SOA [t(6036) = 2.19,
P = 0.028; and t(6036) = 2.76, P = 0.006, respectively]. In
addition, RTs for the UR condition were significantly faster
than the RTs for the RR condition at 600 ms SOA [t(6036) =
2.51, P = 0.012] for the PD group. No other comparisons
were significant.
Further comparisons were also conducted within each
group, in order to determine whether the magnitude of
priming effects for each related condition differed across
SOA. Hence, the magnitude of each significant priming
effect was calculated as the dependent variable, and pairwise
comparisons were then conducted between each SOA for
the different prime conditions. Analysis of the PD group’s
data did not reveal any significant differences in the
magnitude of priming. In contrast, analysis of the control
group’s data revealed that the magnitude of the RR priming
effect at 250 ms SOA was significantly larger than at 1200
ms SOA [t(6036) = 2.72, P = 0.023] and that the
magnitude of the UR priming effect at 250 ms SOA was
significantly larger than at both 600 ms and 1200 ms SOA
[t(6036) = 2.08, P = 0.038; and t(6036) = 2.98, P =
0.003, respectively].
3.2. PD group-good versus poor comprehenders
The PD patients were divided into good versus poor
comprehenders, based on their accuracy to the auditory
comprehension probe questions. Specifically, any PD
patient with a mean OR sentence comprehension score
more than two standard deviations below the group mean
comprehension score for the SR sentences was classified as
a poor comprehender. Similarly, those patients with mean
OR sentence comprehension scores within two standard
deviations of the group mean for SR sentences were
classified as good comprehenders. As a result, seven
patients were classified as poor comprehenders, and 13
patients were classified as good comprehenders. For the
poor comprehenders, motor symptoms were predominantly
left-sided for one, right-sided for three, and bilateral for
three patients. Further, while one of these patients was not
medicated, all other patients were taking levodopa (M
445.83 mg, SD 289.14) and two were also taking Cabaser
(M 2.50 mg, SD 2.12). For the good comprehenders, motor
symptoms were predominantly left sided for five, right sided
for two, and bilateral for patients. Twelve of these patients
were taking levodopa (M 687.50 mg, SD 376.06) and five
were taking Cabaser (M 1.60 mg, SD 1.34). Table 3
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
Table 3
Demographics for the poor and good PD comprehenders
Group
Age
Education
DRS-2
Disease duration
Disease severity
SR comprehension
OR comprehension
Poor comprehenders
Good comprehenders
65.14
10.71
138.86
3.71
2.07
10.00
5.86
63.85
11.92
139.46
5.38
2.08
10.62
9.15
(4.26)
(3.50)
(1.86)
(2.63)
(0.67)
(1.15)
(1.46)
(5.09)
(2.22)
(2.26)
(3.18)
(0.53)
(1.56)
(1.41)
Standard deviations in parentheses.
Abbreviations: DRS-2, Dementia Rating Scale-2; SR, subject relative; OR,
object relative.
illustrates the demographics and mean comprehension
scores for the two subgroups. The PD patient subgroups
differed in their comprehension accuracy to OR sentence
comprehension probes [t(18) = 4.94, P < 0.001] but did
not differ in their comprehension of SR sentence comprehension probes. The PD patient subgroups were not
significantly different in terms of age, education, disease
severity, or disease duration, and did not differ significantly
on any of the individual DRS-2 [31] subscores or on the
DRS-2 total score.
Analyses of the two subgroups were conducted using
mixed linear model analyses with subject as a random
factor, group (good/poor comprehender) as a betweensubjects factor, SOA and prime as within-subject factors,
and position as a covariate. Table 4 displays the mean RTs
(covaried for position of target presentation) for the good
and poor comprehenders as a function of SOA and prime.
The results revealed a significant main effect of SOA
[ F(2,2778) = 35.57, P < 0.001], significant interaction
effects of Group SOA and SOA Prime [ F(2,2778) =
5.11, P = 0.006; and F(6,2778) = 3.69, P = 0.001,
respectively], and a main covariate effect of position
[ F(1,2778) = 46.28, P < 0.001]. Once again, planned
pairwise comparisons were conducted to further investigate
the pattern of priming across time for the two groups.
Analysis of the good comprehender’s data revealed
significant RR and UR priming effects at 250 ms SOA
[t(2778) = 2.10, P = 0.035; and t(2778) = 3.10, P =
0.002, respectively], and significant RU and UR priming
85
effects at 600 ms SOA [t(2778) = 2.33, P = 0.02; and
t(2778) = 2.54, P = 0.01, respectively]. No significant
priming effects were evident, however, at 1200 ms SOA. In
contrast, analysis of the poor comprehender’s data revealed
no significant priming effects at the 250-ms and 600-ms
SOA, although priming effects for the UR condition at the
600-ms SOA were just outside significance ( P = 0.05).
Furthermore, a significant negative priming effect was
evident for the UR condition [t(2778) = 2.46, P = 0.014]
at 1200 ms SOA.
Consistent with the analyses conducted earlier, planned
pairwise comparisons were also used to compare the RTs for
each of the related prime conditions. Analysis of the good
comprehender’s data did not reveal any significant differences in RT for any prime condition. In contrast, analysis of
the poor comprehender’s data revealed that the RTs for the
RR condition were faster than the RTs for the RU condition
at 250 ms SOA [t(2778) = 2.27, P = 0.023], and the RTs
for the UR condition were significantly greater than the RTs
for the RR condition at 600 ms SOA [t(2778) = 2.41, P =
0.016]. No other significant differences were evident.
Further comparisons to investigate whether the magnitude
of semantic priming effects for each condition differed
across SOA were also conducted, but no significant differences were evident.
4. Discussion
The present study used a multi-priming paradigm to
assess the integrity of semantic activation across time in PD
and controls. The results revealed a different pattern of
semantic priming at the 250-ms and 1200-ms SOAs for the
PD group, compared to the control group, suggesting that
both automatic and controlled aspects of semantic processing may be compromised in PD. These findings are
considered in terms of a reduced signal-to-noise ratio and/
or reduced semantic inhibition, resulting from disturbances
to the frontal – striatal system in PD. Another result worthy
of note was the unexpected absence of priming in the RR
condition at 600 ms SOA for both groups. This result may
have implications for the dual influence of both automatic
and controlled processes, which may be differentially
Table 4
Mean RTs for the poor comprehenders and good comprehenders as a function of SOA and Prime condition
Prime condition
Group
Good comprehenders (n = 13)
Poor comprehenders (n = 7)
SOA
SOA
250
Related – related
Related – unrelated
Unrelated – related
Unrelated – unrelated
625
632
613
648
600
(114)
(116)
(114)
(121)
603
595
592
621
(114)
(84)
(93)
(115)
RTs reported in milliseconds; standard deviations in parentheses.
Abbreviations: SOA, stimulus onset asynchrony.
1200
250
626
635
634
643
640
674
648
665
(106)
(115)
(115)
(109)
600
(127)
(128)
(134)
(124)
625
601
588
618
1200
(137)
(95)
(103)
(123)
628
628
657
620
(118)
(119)
(153)
(118)
86
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
utilized across the two prime words. A further aim of the
present study was to compare the time course of semantic
activation in PD patients with good versus poor comprehension of noncanonical sentences. An absence of semantic
priming effects at 250 ms SOA was evident for the subgroup
of PD patients with poor comprehension. This result is
consistent with suggestions that slowed information processing speed may be linked to the sentence comprehension
deficits evident in some patients with PD [24,36].
significant UR priming effect, but an absence of any RU
priming effect. This result is not necessarily unexpected,
however, since Balota et al. [6] have demonstrated that
under conditions of brief prime presentation, older adults
produce larger attentional or expectancy based priming
effects at a medium, as opposed to a longer SOA. Hence, the
apparent reduction in controlled processing evident in the
present study may be related to the short 100 ms prime
duration.
4.1. Semantic activation in controls
4.2. Semantic activation in PD
Analysis of the results for the control group illustrated
different semantic priming effects across the three prime
conditions and SOAs. At 250 ms SOA, priming effects for
all prime conditions were significant, although the magnitude of RU priming was significantly smaller than the
magnitude of RR and UR priming. This smaller magnitude
of RU priming is consistent with the results of Balota and
Paul’s [5] experiment using associatively related word pairs.
Interestingly, this effect appears to be merely indicative of
the rapid decay in automatic semantic activation, as opposed
to any interference created by the intervening unrelated
word. Specifically, it is evident that the magnitude of the UR
priming effect at 600 ms SOA is similar to that of the RU
priming effect at 250 ms SOA (Table 2). Given that the
elapsed time between presentation of the related prime and
presentation of the target is similar for both the RU (at 250
ms SOA) and UR (at 600 ms SOA) conditions, the lower
magnitude of priming for the RU condition appears
consistent with a time related decay in the strength of
semantic activation.
It is also worthy of note that despite significant priming
for the RR condition, inspection of Table 2 illustrates that
the magnitude of priming for the RR condition is not
significantly different to that of the UR condition. Thus, it
appears reasonable to conclude that a summation of priming
did not occur for this condition. Although this finding may
be consistent with the results of Chenery et al. [14], it is at
odds with other research that has demonstrated summation
priming [5,41]. Consequently, the effect of multiple related
primes on automatic semantic activation appears to be
difficult to establish.
While the results at 250 ms SOA provide an indication of
automatic semantic activation, controlled semantic processing may be expected to emerge at longer SOAs [44].
Therefore, analysis of the results at 600 ms SOA may
provide an indication of the time course of both automatic
and controlled semantic processes. For instance, the
significant priming for the UR condition at 600 ms SOA
may still reflect automatic semantic activation, but the
significant RU priming effect may reflect the emergence of
controlled processes. As noted previously, there was no RR
priming at 600 ms SOA, a feature that will be discussed in
Section 4.3. By 1200 ms SOA, the results suggest that
controlled semantic processing may be diminishing, with a
Analysis of the results for the PD group across SOAs
illustrated a different pattern of priming effects to that of the
control group. At 250 ms SOA, the UR and RR priming
effects were significant for the PD group and the similar
magnitude of priming for these conditions suggested that
summation priming did not occur. More importantly,
however, the RU priming effect was not significant. Given
that the UR priming effect at 600 ms SOA is still significant
in PD, this absence of priming in the RU condition at 250
ms SOA cannot be explained merely by the increased time
between the related prime and target, and so is not consistent
with a rapid decay in semantic activation. Rather, the results
indicate a disruption to semantic activation in the RU
condition at 250 ms SOA. Thus, as predicted, the disruption
to semantic priming appears to occur independently of any
delays to the onset of semantic activation and may reflect a
generalized change to information processing in PD that is
consistent with dopamine depletion.
It has been suggested that dopamine can increase the
signal-to-noise ratio by integrating relevant information and
screening out less relevant information [14]. As we have
previously argued [2], therefore, the absence of semantic
priming in the RU condition for the PD group of the present
study may be related to a reduced signal-to-noise ratio of
information processing. Specifically, a reduced signal-tonoise ratio in PD may decrease the salience of a related
prime word (the signal) and increase the salience of an
unrelated prime word (the noise). As a result, the presence
of an intervening unrelated word in the RU condition may
reduce the salience of the related prime word, thereby
disrupting semantic activation. It is important to note that
difficulties with semantic inhibition [26] and difficulties
attending to relevant stimuli and ignoring irrelevant stimuli
[37] have also been observed in PD. Hence, if the salience
of an unrelated prime word is increased in PD, then
difficulties inhibiting the influence of this unrelated prime
word may ensue. As a result of this reduced inhibition,
semantic activation may be disrupted in the RU condition.
Thus, a reduced signal-to-noise ratio and decreased semantic inhibition in PD may have an interactive effect, both
contributing to a disruption of semantic activation across an
unrelated prime word. Interestingly, the rapid rise in
magnitude of priming for the RU condition at 600 ms
SOA (Table 2), which is likely to reflect the influence of
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
some controlled processing, also indicates that any influence
of the intervening unrelated word is specific to automatic
semantic processes.
In addition to its influence on signal-to-noise ratio’s,
dopamine may also be expected to influence the speed of
information processing. For instance, automatic semantic
activation appears to decay more quickly for healthy
individuals in a hyperdopaminergic state [3]. Accordingly,
a hypodopaminergic state in PD may be expected to induce
a slower than normal decay in automatic semantic activation. Indeed, while the magnitude of priming for the UR
condition in the control group decreases significantly from
the 250-ms to the 600-ms SOA, the magnitude of priming
for the PD group does not (Table 2). These findings are
consistent with the results of previous studies [4,24] and
suggest that the peak level of automatic semantic activation
is sustained over a longer period of time for the PD group. A
slower decay in semantic activation was not observed for
the RU and RR conditions, however, since semantic
activation may be disrupted in both these conditions.
Specifically, the presence of the intervening unrelated word
in the RU condition may disrupt semantic activation in PD
at 250 ms SOA. Further, as discussed in Section 4.3, the
presence of two related prime words in the RR condition
may also disrupt semantic activation at 600 ms SOA.
Interestingly, changes to controlled processing are also
evident from the results of the present study. Despite
evidence of what appears to be some controlled processing
at 600 ms SOA, all priming effects are eliminated by 1200
ms SOA for the PD group, suggesting a decline in
controlled processing at longer SOAs. Researchers have
suggested, however, that frontal – striatal dysfunction may
impair attention-based access to the semantic network
[17,21]. Given the connections between the striatum and
the frontal lobes [1], therefore, compromised frontal – striatal
functioning in PD may explain the disturbances to
controlled processing evident in the present study.
4.3. RR condition at 600 ms SOA
Interestingly, for both the PD and control group, the
priming effect for the RR condition at 600 ms SOA is not
significant, with the substantial drop in magnitude of
priming from 250 ms to 600 ms SOA at variance with the
significant priming effects for the RU and UR conditions.
To our knowledge, while previous research using the multipriming paradigm has not illustrated a similar effect for the
RR condition, neither has this research tested the integrity of
priming for the RR condition at a similar 600 ms SOA.
Instead, researchers have typically used both a short and a
long SOA [5,41], such that priming effects obtained
probably only reflect either automatic or controlled processes. Thus, while priming effects observed in the RR
condition at the 250-ms and 1200-ms SOAs of the present
study may reflect the influence of automatic semantic
activation or controlled semantic processes respectively,
87
interpretation of the priming effects at the 600-ms SOA is
more difficult. Specifically, while the influence of P1 on
the target at 600 ms SOA may reflect controlled semantic
processes, the influence of P2 on the target is most likely a
result of automatic semantic activation. Hence, the absence
of priming in the RR condition at 600 ms SOA may be
caused by some kind of interference. For instance, the
controlled semantic processing from P1 to the target may
disrupt or be disrupted by the automatic semantic activation induced by P2, thereby resulting in an absence of
priming.
The results of the control group at 1200 ms SOA provide
further support for this argument. In particular, at 1200 ms
SOA, both P1 and P2 may induce controlled semantic
processing, which would not be expected to interfere with
semantic activation in the RR condition. Indeed, RR
priming is significant at 1200 ms SOA for the control
group. Nonetheless, theories of interference in the RR
condition at 600 ms SOA must remain speculative until
further research is conducted.
4.4. Semantic activation in PD—good versus poor
comprehenders
Division of the PD patients into those with good versus
poor comprehension of OR sentences reveals a different
pattern of priming for each subgroup. The pattern of priming
effects for the good comprehenders at each SOA illustrates a
similar time course of semantic activation as that identified
following analysis of the whole PD group. Thus, the results
illustrate automatic semantic activation at 250 ms SOA, and
aberrant controlled processing at 1200 ms SOA for the good
comprehenders. More importantly, however, the results also
demonstrate that even the PD patients with intact comprehension of noncanonical sentences fail to show priming for
the RU condition at the 250-ms SOA. Accordingly, this
result provides further support for our argument that the
presence of an intervening unrelated word can disrupt the
integrity of automatic semantic activation in PD, without
concurrent delays in the time course of semantic activation
or impaired comprehension of complex sentences.
In contrast to the good comprehenders, analysis of the
poor comprehender’s data revealed no significant priming
effects for any prime condition at 250 ms SOA, while the
UR priming effect was just outside significance at 600 ms
SOA. Hence, these results are consistent with previous
findings of delayed semantic activation only in PD patients
with poor comprehension of noncanonical sentences [24]. It
is important to note, however, that the magnitude of the RR
priming effect at 250 ms SOA is in fact marginally larger for
the poor comprehenders of the present study, compared to
the good comprehenders (Table 4). The absence of
significant RR priming for the poor comprehenders, therefore, may simply reflect the low number of subjects and
suggests that the presence of two related prime words may
partially enhance the spread of semantic activation for these
88
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
patients. Further research with larger subject numbers will
be needed to confirm this hypothesis.
The results also highlight an interesting distinction
between the two subgroups of PD participants. Specifically,
while the good comprehenders present primarily with a
deficit in controlled semantic processes, the poor comprehenders present with a deficit in both controlled and
automatic semantic activation. Recently, Grossman et al.
[24] suggested that the dopamine dependent frontal –striatal
system might be responsible for maintaining an adequate
speed of lexical activation during sentence processing,
which is consistent with observations of reduced striatal
recruitment in PD during the processing of complex
noncanonical sentences [25]. Therefore, the delays in
automatic semantic activation evident in the present study
may be related to compromised frontal–striatal function.
Nonetheless, explaining why only a subgroup of PD
patients present with delayed semantic activation and
sentence processing deficits is difficult. Grossman et al.
[24] suggested that such variability in performance might be
related to the level of dopamine deficiency. Thus, it is
possible that mild levels of dopamine depletion in good
comprehenders are sufficient to disrupt controlled semantic
processes, while leaving the time course of automatic
semantic activation relatively intact. In contrast, dopamine
depletion may be more advanced in PD patients with poor
comprehension of noncanonical sentences, resulting in an
additional disruption to the speed of information processing,
evidenced by a delayed time course of automatic semantic
activation. Accordingly, if sentence comprehension is linked
to the integrity of information processing speed, then
increased dopamine depletion will be expected to impair
complex sentence comprehension.
The influence of dopamine depletion on sentence
comprehension in PD, however, is by no means clear.
Although there have been findings of improved comprehension in PD patients while on dopaminergic supplementation [23], other research has failed to find any change to
sentence comprehension in PD patients when Fon_ and Foff_
this medication [51]. Thus, future research that compares
sentence comprehension and/or semantic priming in PD
patients Fon_ and Foff_ dopaminergic supplementation may
shed further light on the potential influence of dopamine on
the mechanisms of lexical access.
One final point is that an unexpected negative UR
priming effect was evident for the poor comprehenders at
1200 ms SOA. Negative priming effects have often been
interpreted in terms of a center-surround mechanism [10],
which supposedly facilitates retrieval of a weakly activated
prime word by dampening the activation of closely related
semantic representations. If the poor comprehenders
encountered difficulty activating prime words at 1200 ms
SOA, however, negative RU and RR priming effects may
also be expected. Given that negative priming was not
observed for these prime conditions, application of the
center – surround theory to the results of the present study
may not be warranted. Therefore, the reasons for the
negative priming effect remain unknown.
5. Conclusions
The present study investigated the integrity of semantic
activation over time in patients with PD and healthy
controls, revealing a different pattern of both automatic
and controlled semantic processing for the two groups.
From the results presented, it is proposed that the presence
of an intervening unrelated word interferes with automatic
semantic activation in PD, due to a reduction in the signalto-noise ratio of information processing and/or decreased
semantic inhibition. Furthermore, the results of the present
study are also consistent with a disruption to the formation
of controlled or attention based processes at longer SOAs in
patients with PD. Apart from generalized semantic processing deficits, the results also supported a delayed time course
of semantic activation in PD patients with poor comprehension of noncanonical sentences. These findings lend
further support to the notion that slowed information
processing may contribute to the sentence processing
deficits evident in some patients with PD.
Acknowledgments
This research was supported by participants from the 50+
Registry of the Australasian Centre on Ageing, The
University of Queensland.
References
[1] G.E. Alexander, M.D. Crutcher, M.R. DeLong, Basal ganglia –
thalamocortical circuits: parallel substrates for motor, oculomotor,
‘‘prefrontal’’ and ‘‘limbic’’ functions, Prog. Brain Res. 85 (1990)
119 – 146.
[2] A.J. Angwin, H.J. Chenery, D.A. Copland, B.E. Murdoch, P.A.
Silburn, Summation of semantic priming in Parkinson’s disease and
healthy individuals, Brain Lang. 87 (2003) 96 – 97.
[3] A.J. Angwin, H.J. Chenery, D.A. Copland, W.L. Arnott, B.E.
Murdoch, P.A. Silburn, Dopamine and semantic activation: an
investigation of masked direct and indirect priming, J. Int. Neuropsychol. Soc. 10 (2004) 15 – 25.
[4] W.L. Arnott, H.J. Chenery, B.E. Murdoch, P.A. Silburn, Semantic
priming in Parkinson’s disease: evidence for delayed spreading
activation, J. Clin. Exp. Neuropsychol. 23 (2001) 502 – 519.
[5] D.A. Balota, D.A. Paul, Summation of activation: evidence from
multiple primes that converge and diverge within semantic memory,
J. Exp. Psychol., Learn. Mem. Cogn. 22 (1996) 827 – 845.
[6] D.A. Balota, S.R. Black, M. Cheney, Automatic and attentional
priming in young and older adults: reevaluation of the two-process
model, J. Exp. Psychol. Hum. Percept. Perform. 18 (1992) 485 – 502.
[7] K.A. Bayles, M.W. Trosset, C.K. Tomoeda, E.B. Montgomery, J.
Wilson, Generative naming in Parkinson’s disease patients, J. Clin.
Exp. Neuropsychol. 15 (1993) 547 – 562.
[8] M.W. Bondi, A.W. Kaszniak, K.A. Bayles, K.T. Vance, Contributions
of frontal system dysfunction to memory and perceptual abilities in
Parkinson’s disease, Neuropsychology 7 (1993) 89 – 102.
A.J. Angwin et al. / Cognitive Brain Research 25 (2005) 78 – 89
[9] D.B. Calne, B.J. Snow, C. Lee, Criteria for diagnosing Parkinson’s
disease, Ann. Neurol. 32 (1992) S125 – S127.
[10] T. Carr, T. Dagenbach, Semantic priming and repetition priming from
masked words: evidence for a center-surround attentional processes in
perceptual recognition, J. Exp. Psychol., Learn. Mem. Cogn. 16
(1990) 341 – 350.
[11] Cedrus, Superlab Experimental Laboratory Software, Cedrus Corporation, Phoenix, 1996.
[12] C. Cepeda, M.S. Levine, Dopamine and N-methyl-d-aspartate
receptor interactions in the neostriatum, Dev. Neurosci. 20 (1998)
1 – 18.
[13] H.J. Chenery, A. Holmes, J.C.L. Ingram, E.A. Cardell, Temporal
constraints on summation of activation in Broca’s aphasia: evidence
from a triplet priming task, Brain Lang. 87 (2003) 99 – 100.
[14] H.J. Chenery, D.A. Copland, J. McGrath, G. Savage, Maintaining
and updating semantic context in schizophrenia: an investigation of
the effects of multiple remote primes, Psychiatry Res. 126 (2004)
241 – 252.
[15] N. Chomsky, Lectures on Government and Binding, Dordrecht, Foris,
1981.
[16] A.M. Collins, E.F. Loftus, A spreading activation theory of semantic
processing, Psychol. Rev. 82 (1975) 407 – 428.
[17] D.A. Copland, The basal ganglia and semantic engagement: potential
insights from semantic priming in individuals with subcortical
vascular lesions, Parkinson’s disease, and cortical lesions, J. Int.
Neuropsychol. Soc. 9 (2003) 1041 – 1052.
[18] D.A. Copland, H.J. Chenery, B.E. Murdoch, Understanding ambiguous words in biased sentences: evidence of transient contextual
effects in individuals with nonthalamic subcortical lesions and
Parkinson’s disease, Cortex 36 (2000) 601 – 622.
[19] J.V. Filoteo, F.J. Friedrich, L.M. Rilling, J.D. Davis, J.L. Stricker, M.
Prenovitz, Semantic and cross-case identity priming in patients with
Parkinson’s disease, J. Clin. Exp. Neuropsychol. 25 (2003) 441 – 456.
[20] H.L. Geyer, M. Grossman, Investigating the basis for the sentence
comprehension deficits in Parkinson’s disease, J. Neurolinguist. 8
(1995) 191 – 205.
[21] M. Gold, S.E. Nadeau, D.H. Jacobs, J.C. Adair, L.J. Gonzalez-Rothi,
K.M. Heilman, Adynamic aphasia: a transcortical motor aphasia
with defective semantic strategy formation, Brain Lang. 57 (1997)
374 – 393.
[22] M. Grossman, J. Kalmanson, N. Bernhardt, J. Morris, M.B. Stern, H.I.
Hurtig, Cognitive resource limitations during sentence comprehension
in Parkinson’s disease, Brain Lang. 73 (2000) 1 – 16.
[23] M. Grossman, G. Glosser, J. Kalmanson, J. Morris, M.B. Stern, H.I.
Hurtig, Dopamine supports sentence comprehension in Parkinson’s
disease, J. Neurol. Sci. 184 (2001) 123 – 130.
[24] M. Grossman, E. Zurif, C. Lee, P. Prather, J. Kalmanson, M.B. Stern,
H.I. Hurtig, Information processing speed and sentence comprehension in Parkinson’s disease, Neuropsychology 16 (2002) 174 – 181.
[25] M. Grossman, A. Cooke, C. DeVita, C. Lee, D. Alsop, J. Detre, J. Gee,
W. Chen, M.B. Stern, H.I. Hurtig, Grammatical and resource
components of sentence processing in Parkinson’s disease: an fMRI
study, Neurology 60 (2003) 775 – 781.
[26] J.M. Gurd, R.M. Oliveira, Competitive inhibition models of lexicalsemantic processing: experimental evidence, Brain Lang. 54 (1996)
414 – 433.
[27] P. Hagoort, Processing of lexical ambiguities: a comment on Milberg,
Blumstein, and Dworetzky (1987), Brain Lang. 36 (1989) 335 – 348.
[28] D.L. Harrington, K.Y. Haaland, N. Hermanowicz, Temporal processing in the basal ganglia, Neuropsychology 12 (1998) 3 – 12.
[29] T.M. Hines, B.T. Volpe, Semantic activation in patients with
Parkinson’s disease, Exp. Aging Res. 11 (1985) 105 – 107.
[30] M.M. Hoehn, M.D. Yahr, Parkinsonism: onset, progression, and
mortality, Neurology 17 (1967) 427 – 442.
[31] P.J. Jurica, C.L. Leitten, S. Mattis, Dementia Rating Scale-2.
Professional Manual, Psychological Assessment Resources, Inc., Lutz,
FL, 2001.
89
[32] D. Kemmerer, Impaired comprehension of raising-to-subject constructions in Parkinson’s disease, Brain Lang. 66 (1999) 311 – 328.
[33] U. Kischka, Th. Kammer, S. Maier, M. Weisbrod, M. Thimm, M.
Spitzer, Dopaminergic modulation of semantic network activation,
Neuropsychologia 34 (1996) 1107 – 1113.
[34] G.R. Kiss, C. Armstrong, R. Milroy, J. Piper, An associative thesaurus
of English and its computer analysis, in: A.J. Aitken, R.W. Bailey, N.
Hamilton-Smith (Eds.), The Computer and Literacy Studies, University Press, Edinburgh, 1973.
[35] H. Kucera, W. Francis, Computational Analysis of Present-Day
American English, Brown Univ. Press, Providence, RI, 1967.
[36] C. Lee, M. Grossman, J. Morris, M.B. Stern, H.I. Hurtig, Attentional
resource and processing speed limitations during sentence processing
in Parkinson’s disease, Brain Lang. 85 (2003) 347 – 356.
[37] B.E. Levin, M.M. Llabre, W.J. Weiner, Cognitive impairments
associated with early Parkinson’s disease, Neurology 39 (1989)
557 – 561.
[38] C. McDonald, G.G. Brown, J.M. Gorell, Impaired set-shifting in
Parkinson’s disease: new evidence from a lexical decision task, J. Clin.
Exp. Neuropsychol. 18 (1996) 793 – 809.
[39] P. McNamara, M. Krueger, K. O’Quin, J. Clark, R. Durso,
Grammaticality judgements and sentence comprehension in Parkinson’s disease: a comparison with Broca’s aphasia, Int. J. Neurosci. 86
(1996) 151 – 166.
[40] W. Milberg, K.L. Sullivan, S.E. Blumstein, Summation of semantic
priming effects in aphasia: deficits in the integration of activation are
related to disorders of language, Brain Lang. 65 (1998) 76 – 78.
[41] W. Milberg, S. Blumstein, K.S. Giovanello, C. Misiurski, Summation
priming in aphasia: evidence for alterations in semantic integration and
activation, Brain Cogn. 51 (2003) 31 – 47.
[42] D. Natsopoulos, Z. Katsarou, S. Bostantzopoulou, G. Grouios, G.
Mentenopoulos, J. Logothetis, Strategies in comprehension of relative
clauses by Parkinsonian-patients, Cortex 27 (1991) 255 – 268.
[43] D. Natsopoulos, G. Grouios, S. Bostantzopoulou, G. Mentenopoulos,
Z. Katsarou, J. Logothetis, Algorithmic and heuristic strategies in
comprehension of complement clauses by patients with Parkinsonsdisease, Neuropsychologia 31 (1993) 951 – 964.
[44] J.H. Neely, Semantic priming and retrieval from lexical memory: roles
of inhibitionless spreading activation and limited-capacity attention,
J. Exp. Psychol. Gen. 106 (1977) 226 – 254.
[45] J.H. Neely, Semantic priming effects in visual word recognition: a
selective review of current findings and theories, in: D. Besner, G.W.
Humphreys (Eds.), Basic Processes in Reading: Visual Word
Recognition, Lawrence Erlbaum, Hillsdale, NJ, 1991, pp. 264 – 333.
[46] A. Nieoullon, Dopamine and the regulation of cognition and attention,
Prog. Neurobiol. 67 (2002) 53 – 83.
[47] R.A. Poldrack, E. Temple, A. Protopapas, S. Nagarajan, P. Tallal, M.
Merzenich, et al., Relations between the neural bases of dynamic
auditory processing and phonological processing: evidence from
fMRI, J. Cogn. Neurosci. 13 (2001) 687 – 697.
[48] C. Randolph, A.R. Braun, T.E. Goldberg, T.N. Chase, Semantic
fluency in Alzheimer’s, Parkinson’s, and Huntington’s disease:
dissociation of storage and retrieval failures, Neuropsychology 7
(1993) 82 – 88.
[49] R.I. Schubotz, A.D. Friederici, D.Y. von Cramon, Time perception and
motor timing: a common cortical and subcortical basis revealed by
fMRI, NeuroImage 11 (2000) 1 – 12.
[50] D. Servan-Schreiber, H. Printz, J.D. Cohen, A network model of
catecholamine effects: gain, signal-to-noise ratio, and behaviour,
Science 249 (1990) 892 – 896.
[51] R.L. Skeel, B. Crosson, S.E. Nadeau, J. Algina, R.M. Bauer, E.B.
Fennell, Basal ganglia dysfunction, working memory, and sentence
comprehension in patients with Parkinson’s disease, Neuropsychologia 39 (2001) 962 – 971.
[52] K.B. Spicer, G.G. Brown, G.M. Gorell, Lexical decision in Parkinson’s disease: lack of evidence of generalized bradyphrenia, J. Clin.
Exp. Neuropsychol. 16 (1994) 457 – 471.