Semantic processing deficits

in patients with Parkinson's disease:

degraded representation or defective retrieval?
Paul A. Watters, MAPS; Malti Patel, PhD
Watters, Patel
Department of Computing, School of Mathematics, Physics, Computing and Electronics, Macquarie
University, Sydney, Australia

Objective: To determine whether degraded representations (characterized by small differences between

word sense frequencies), or defective competitive processes (high levels of word sense lateral inhibition),
individually or jointly, can give rise to parkinsonian semantic deficits. Design: Computer model of smeantic processing. Outcome measures: Correct sense selection, defined by the activation of the word sense
unit that first reaches the 0.5 activation threshold. If Parkinson disease (PD)-like errors are observed only at
high levels of lateral inhibition, independently of low or high sense frequency deltas (SFDs), this would indicate that a defective competitive process alone could account for the errors. Alternatively, if PD-like errors
were observed at any level of lateral inhibition, exclusively with low SFD words, this would indicate that
degraded representations alone could account for the errors. Results: Neither degraded representations
nor defective competitive processes alone can account for parkinsonian semantic errors. An interaction
between the 2, however, correctly reproduces both increased errors and longer latency responses.
Conclusions: Competing explanations for semantic deficits in patients with Parkinson's disease need to
be integrated in order to develop effective interventions (e.g., estimating the amount of context required
to improve semantic processing performance).
Objectif: Determiner si des representations sont degradees (caracterisees par de faibles differences entre
les frequences du sens des mots), ou des processus concurrentiels deficients (niveaux eleves d'inhibition
laterale du sens des mots) peuvent, individuellement ou collectivement, provoquer des deficits semantiques
parkinsoniens. Conception : Modele informatise de traitement semantique. Mesures de resultats:
Selection du sens approprie, defini par l'activation de l'unite du sens du mot qui est la premiere a atteindre le seuil d'activation 0,5. Si l'on observe des erreurs ressemblant a un deficit parkinsonien a des niveaux
eleves d'inhibition laterale seulement, peu importe que les differences entre les frequences du sens (SFD)
soient faibles ou elevees, cela indiquerait qu'un processus concurrentiel defectueux pourrait a lui seul expliquer les erreurs. Par ailleurs, si l'on observe des erreurs ressemblant a un deficit parkinsonien a n'importe
quel niveau d'inhibition laterale, exclusivement avec des mots a faible SFD, cela indiquerait que des

Correspondence to: Paul Watters, Department of Computing, School of Mathematics, Physics, Computing and Electronics,
Macquarie University, Sydney NSW 2109 Australia; fax 61 2 9850 9551
Medical subject headings: computer simulation; dopamine; neural networks (computer); Parkinson disease; semantics
J

Psychiatry Neurosci 1999;24(4):322-32.

Submitted Apr. 17, 1998

Revised Oct. 8, 1998
Accepted Jan. 4, 1998

( 1999 Canadian Medical Association

322
322S

neuroscience
psychiatrie
de
Revue
6science
Rie
;li" t, et
if ddee vear
de psy
4,

ol

Vol.

iE& 21^4:ii01
60
1:9f

Smantk pro.esst.g Iti

representations degradees pourraient expliquer a elles seules les erreurs. Resultats: Ni les representations
degradees ni les processus concurrentiels deficients peuvent a eux seuls expliquer les erreurs semantiques parkinsoniennes. Une interaction entre les deux phenomenes reproduit toutefois correctement a la fois des erreurs
accrues et des reactions a latence plus longue. Conclusions: 11 faut integrer des explications differentes des
deficits semantiques chez les patients atteints de la maladie de Parkinson afin de mettre au point des interventions efficaces (p. ex., estimer l'importance du contexte necessaire pour ameliorer le rendement du traitement
semantique).

Parkinson's disease
and semantic processing
Parkinson's disease (PD) is an organic brain disorder
that arises from the degeneration of neural pathways in
the extrapyramidal motor system, and is commonly
associated with a marked reduction in motor performance. Atrophy of the neurons of the substantia nigra
give rise to motor dysfunction,' such as resting tremor,
which is the first symptom usually reported to physicians by patients with PD.2 However, as Brod et all have
highlighted, problems associated with PD are not
restricted to motor symptoms; patients often feel that
clinicians do not pay sufficient attention to the cognitive
and psychological problems associated with PD.
The distinction between motor and nonmotor disturbances in patients with PD appears to be justified
impairments in language and cognitive processing in
patients with PD have increasingly elicited the interest
of both neurologists and neuropsychologists. This is
largely owing to recent physiological evidence that linguistic and cognitive impairments in patients with PD
might arise from disturbances in dopaminergic systems
that lie outside the extrapyramidal system. For example, Javoy-Agid and Agid' found a reduction in net
dopamine levels in the mesolimbic forebrain, a region
with extensive projections into key prefrontal areas and
in the association areas of the neocortex, in patients
with PD.5 As many as 5 different dopaminergic loops,
all involving frontal lobe circuits, might exhibit damage
in patients with PD, potentially giving rise to a complex
set of observed cognitive and linguistic performance
deficits.6

Historically, tests of language ability and language

performance were performed only to indicate cognitive
deficits in patients with PD who had undergone
surgery to reduce motor symptoms.7 However, interest
in language-processing disorders is not a historical oddity; assessments of verbal fluency in patients with PD in
recent years have clearly demonstrated that lexical proVol. 24, no4
V6.21
w 4 1999
_-

cessing deficits are distinguishable from more obvious

speech impairments associated with motor dysfunction. This supports the view that stuttering, which arises from lesions in the substantia nigra, has a separate
physiological basis from specifically linguistic deficits.
For example, patients with PD have shorter speech
duration and greater time per pause than control subjects.8 However, these patients also have problems with
nonmotor speech production, generating a higher proportion of open class optional phrases in verbal discourse, for example, when compared with control subjects.9 Further exploration of linguistic deficits in
patients with PD indicate that, even in the early stages
of the disease, patients show reduced sentence length
and information content, but normal syntactic complexity in speech production.'0
It is thought that the reduction in information content
can be attributed specifically to lexical-semantic processing. For example, many patients experience difficulty in understanding sentences with lexical-causative
verbs, that is, verbs that signal a new state of affairs."
Lexical impairments in patients with PD also appear to
be specifically associated with semantic processing,
since nonsemantic lexical decisions are often unaffected
in the disorder. Semantic deficit specificity is supported
by the finding that the performance of patients with PD
on word-search tasks not involving a semantic judgement was unimpaired.'2 This indicates that the key
problem lies with semantic memory and access to different word meanings and their categories, and not
with nonsemantic lexical processes (reviewed by
Watters and Gurd13).

Although the results of linguistic performance tests

might be confounded with more general cognitive dysfunction, many studies have actually shown that the
effects can be clearly separated. For example, performance in tasks requiring algorithmic strategies are
more likely to be associated with impairment in verbal
reasoning in patients with PD than performance in
tasks requiring pragmatic or heuristic approaches.'4 In

Jotmialof .sychIat*y &.

.,,,:j,
323

Watters and Paete

addition, although patients with PD are slower than

age-matched controls in performing the Stroop colourword task, the error rates of patients with PD are the
same as controls, effectively ruling out a perceptual or
attentional basis for lexical-semantic processing errors
in PD.1" Lexical-semantic deficits in patients with PD
exist even when global mental status is only mildly
affected.'6 This separation of language processing
deficits from other potential cognitive or perceptual
processing deficits indicates the potential for simple
tests of lexical-semantic performance to be used as an
inexpensive diagnostic tool. In fact, several studies have
already used neuropsychological test batteries, such as
the Montreal-Stanford Neurolinguistic Protocol,"7 to
discriminate between the linguistic errors associated
with patients with PD (syntactically intact utterances)
and patients with Huntington's or Alzheimer's disease
(reduced ability to process syntactic complexity).
The specific reduction in semantic processing performance forms the basis for the so-called "semantic deficit
hypothesis" of PD, which attempts to account for the
increased errors and longer latency responses to semantic judgement tasks in patients with PD compared with
controls.'8 This slowing in semantic processing may be
related to the patients' word-finding impairment in verbal fluency. For example, the time taken to scan a vertical list of words to identify a target (e.g., "any plant")
can be used as a measure of the time taken to select that
item in lexical-semantic memory. These performance
deficits occur in "neutral conditions" when there is
no context or semantic priming
indicating that
patients with PD have a strong dependence on contextual information. When context is absent during the
processing of lexical-semantic information, errors in
performance arise. For example, a recent study by
Spicer et al'9 reported that patients with PD exhibited a
larger difference in response time between a neutral cue
and a category prime condition than controls. When a
target word was preceded by a category cue, the
response was faster than when the target was preceded
by a semantically neutral cue. This supports previous
findings that for patients with PD there is a great dependence on explicit, immediate semantic cues to correctly
process verbal information.20 In other words, a little contextual information can go a long way for patients with
PD since, as reported by Spicer et al,'9 the difference
between performance in context and no-context priming conditions was greater for patients with PD than for
normal control subjects.

324
3A

Since Gurd and Oliveira2' believe that semantic errors

in patients with PD arise from defective competitive
processes involved in inhibiting incorrect responses, it
is difficult to see how the issue can be resolved by performing more neuropsychological tests. However, it
should be noted that not everyone accepts that defective retrieval processes might form the basis for a
semantic deficit in patients with PD. For example, a
recent study found little evidence to support the notion
that differences in response times for neutral and
primed conditions in patients with PD could be
explained by difficulties accessing semantic information.2 Rather, it was suggested that patients with PD
experience difficulty switching from lexical access
strategies appropriate for category prime compared
with neutral conditions, thus producing slower latencies and more lexical errors in the latter condition.
Other studies have shown that performance on free
recall in category naming is affected in patients with
PD, whereas recognition is unaffected;23 this suggests
that representations of semantic information, rather
than semantic retrieval processes, might be damaged.
This is supported by a recent study that found that free
recall by patients with PD was impaired relative to both
younger controls and age-matched non-PD subjects.24
In this paper, we propose an alternative approach to
attempting to discriminate between the possible effects
of damaged representations and defective competitive
processes. One possibility is to use a simpler semantic
decision task that does not have many of the problems
associated with evaluating the results of category
judgement studies. However, inherent variability in
language use and comprehension due to differences in
dialect, vocabulary size, and internal, learned representations of word sense frequencies, naturally give rise to
variability in cognitive performance, potentially biasing
the interpretation of empirical results. In addition,
changing the task under scrutiny would introduce an
extra level of complexity into studies of semantic processing errors, when attempting to lucidly account for
the semantic deficits identified by Gurd.'8
Our proposal does not rely on further cognitive testing or brain imaging, but uses a computer model of
semantic processing to explore the 2 competing
hypotheses of PD-like semantic deficits. A computer
model has an advantage over other experimental methods in that it provides an optimal empirical testbed, acting to reduce population variability both between and
within subjects, which could be obscuring real experi-

'41"..1.11
R.ne.d.a.vd,iatricst.t4eiieivescicnce

Ql.j..^0
v `2.

V0L24,n04,
g.X.fs.

..

t.j

19,,

Semantic processing in Parkinson4<s.eXa

iE

mental effects. A model semantic system is proposed to

test the main effects for each possible explanation of
semantic processing errors - that is, whether degraded
representations or defective processes can give rise to
the observed behaviour. It is also possible that an interaction might arise between these 2 factors, a possibility
that has been extensively explored; for example,
Leplow et aP25 found that both recall and recognition
were affected in patients with PD. A simple semantic
processing task (resolving lexical ambiguity) will be
used as an alternative to the more complex categorical
decision tasks.

A model of semantic processing

A model semantic system is an optimal empirical testbed only if it is psychologically and physiologically
plausible. However, the most difficult aspect of modelling cognitive and neural systems is establishing the
plausibility of model architecture and justifying the simpllfying assumptions often made in using biological
data as parameters. The model and simulations presented in this paper are neither a perfect model for semantic
processing, nor do they perfectly replicate every activity
or characteristic of the human brain. Simplifying
assumptions about brain function limit the scope of the
appllcation of the model, but not to the extent that the
model, when tested under experimental conditions, cannot reveal new insights into cognition and brain function. This general approach to modelling neurological
and psychiatric disorders has been successful in testing
theories of abnormal cognitive processing and accounting for experimental data (reviewed in Galletly et a126).

Developing a psychologically plausible model of

semantic processing also makes some philosophical
assumptions about the nature of meaning (especially
lexical and psychological meaning). While "meaning"
obviously exists in the "environment," and we accept
that the "environment" exists independently of mental
states,27 there are also internal representations of that
meaning stored in the patterns of electrical activity in
the brain. Although this might be a key assumption in
cognitive neuroscience (e.g., the single neuron doctrine
of Barlow28), in fact many philosophers do not accept
that an internal representation of meaning is necessary
or desirable.29 A pragmatic approach is adopted in this
paper, based on psychological evidence that representations of words and their different senses are linked to
visual, tactile, auditory, olfactory and gustatory repre-

AI, W

I, 1,.
1:". M.

4A9*9
4"I
"O
.11

sentations in the brain. It is also assumed that lexical

knowledge and word representations exist in the architecture of cortical neural networks, and the strength of
the connection between neurons in these networks.
This representational view of meaning forms the
basis of the computational semantic system described
in this paper. The semantic system is framed in the context of semantic processing required for accurate reading
for example, homographs require some knowledge of word meaning to retrieve a correct pronunciation. Since semantics are important for reading, and
since there is already a psychologically plausible model
of reading, we have attempted to integrate semantic
systems into the dual-route cascaded model (DRC),
developed by Coltheart et al,70 which has both nonlexical (grapheme-phoneme rules) and nonsemantic lexical
routes to retrieve phonology from orthography. In this
paper, we consider only the integrated lexical-semantic
route of the DRC,31 which is implemented as a competitive neural network in which each word, word sense
and associated semantic features are locally represented
(see Watters32 for a discussion of the plausibility of local
representations). If the word ARM, for example, is presented to the top level of the system (the "word level"),
individual letter detectors in visual space ("A,""R," and
"M") are activated, which in turn activate the appropriate word detector (ARM), as per normal lexical access.
These word representations laterally inhibit each other,
and thus only one word's senses will be activated. The
middle level (the "sense level") is responsible for representing the different senses in which polysemous words
can be used (ARMI and ARM2). Different word senses
also laterally inhibit each other, and there are both excitatory and inhibitory connections between the word
and sense levels. The bottom level (the "feature level")
contains basic semantic feature descriptions associated
with each alternative word sense for polysemous words
(ARMIl-1, ARM1-2, ... ARM1-8). These features do not
laterally inhibit each other, but there are both excitatory
and inhibitory connections between the sense and feature levels.
The semantic features are defined by hypernyms
retrieved from the WordNet lexical reference system
(developed at Princeton University by Professor George
Miller and colleagues, and available for downloading
from www.cogsci.princeton.edu/-wn), which has a lexicon of approximately 168 000 words, 91 600 representations of unique concepts and 345 000 relations, as
derived from analyses of large corpora.33 Although the
325

325

Ai

original decompositional semantic theories used a hierarchical feature model (see Collins and Quillian34), this
approach was shown to be psychologically implausible
when the linear relation between response time and
semantic distance, predicted in semantic judgement
tasks, was not found when taking into account conjoint
frequency."' The proposed solution to this problem is to
retain semantic decomposition by linking semantic features to WordNet hypemyms, but to discard the problematic hierarchy. In addition, there is no assumption
that the association between word senses and semantic
features is an excusive, all-or-none relation it is almost
certainly going to be graded and adaptive, given that
each individual speaker of a natural language has a different vocabulary and different linguistic experiences.
This example is depicted in Fig. 1, with the 2 senses of
ARM: the dominant sense of limb, with an empirically
derived familiarity measure of f = 0.46 and a less-dominant sense as weaponry (f = 0.03). The competitive
processes in the semantic system uses word-sense frequency measures derived from Twilley et al6 to influence
the spread of activation in the network when it retrieves
a word meaning (i.e., without context being provided,
the system retrieves the most dominant word sense). The
semantic features associated with each WordNetretrieved word sense for ARM are shown in Fig. 2.

Degraded representations
and defective processes
To test whether degraded representations or defective
processes can produce PD-like deficits in the model
semantic system, a specification for producing both
types of "damage" needs to be developed. In this study,
degraded semantic representations are realized by
using a sense frequency delta (SFD), which is simply the
difference between word sense frequencies or familiarity measures.37 A word with 2 senses is a low-SFD word
if the difference between the sense frequency or familiarity measures of each sense is low. For example, in the
study by Twilley et al,3 BASS has 2 senses, with the
dominant sense of "fish" having f = 0.16, and the lessdominant sense of "musical instrument" having f =
0.13, giving an SFD = 0.03. BASS is therefore a low-SFD
word, which is used to represent a "damaged" representation in this study. A word with 2 senses is a highSFD word if the difference between the sense frequency
of familiarity measures of each sense is high. For example, BELT has 2 senses, with the dominant sense of "a
piece of clothing" having f = 0.23, and the less-domiSense I
limb
extremity, appendage - (a bodily appendage or appendagelike part)
external body part
body part, member
part - (any part of an animal or plant such as an organ or

extremity)
natural object - (an object occurring naturally; not made by
man)
object, inanimate object, physical object - (a nonliving
entity)
entity - (something having concrete existence; living or
nonliving)

ARM 1-1

ARM 18-

ARM 2-1

ARM 2-1

Fig. 1: The top-down architecture of the semantic system

for the example word ARM, which has 2 senses: a limb (f
= 0.46) and weaponry (f = 0.03). At the top level, a word
detector receives input from letter detectors, which is
then connected to a word sense representation in the
middle level. Each word sense is then associated with a
number of semantic features as the lowest level, which
are

not arranged in any hierarchy.

..'

Revue de

Sense 2
weaponry, arms, implements of war, weapons system
instrumentality - (an artifact that is instrumental in
accomplishing some end)
artifact, article, artefact - (a man-made object)
object, inanimate object, physical object - (a nonliving

entity)
entity - (something having concrete existence; living or

nonliving)
Fig. 2: Semantic features linked with WordNet definitions
for each sense of the example word ARM.

psydiiatrie
et de
a,

Reuroseieuce
suence

Vi
Vol.
24, no 4,A 1999
ia,
.:
-j
fi#eljfli.0![ WI :3t
i'

.S' IW

-:

w}5t

0- ;T

i tf

nant sense of "deal a blow" having f = 0.07, giving an

SFD = 0.16.
For words with 3 senses, the situation is more complicated. The 2-word senses from which the SFD is computed must now be selected - it is necessary to redefine the SFD concept in a more general way. The SFD
for words with 3 or more senses is defined as the difference between the sense frequency of familiarity of the
dominant word sense and the next highest word sense
frequency. For example, the word BOLT has 3 senses: a
"lightning bolt" (f = 0.22), a "screw" (f = 0.18), and
"haste" (f = 0.1), giving an SFD = 0.04, which is low,
even though the difference between the highest and
lowest sense frequency of BOLT is 0.12, which is high.
Alternatively, the word BLUFF has 3 senses: a "pretence" (f = 0.16), a "ridge" (f = 0.03), and a "gramineous
plant" (f = 0.02), giving SFD = 0.13, which is high, even
though the difference between the 2 lowest senses is
SFD = 0.01, which is quite low.
It should be noted that if the dominant word sense for
BLUFF was ignored, then BLUFF with the 2 senses of
"ridge" and "gramineous plant" would be a low-SFD
word, with an SFD = 0.01. In this sense, we can see just
how arbitrary the notion of familiarity is, or perhaps
more correctly, how it is readily subject to change
depending on recent and past experience. There is nothing invariant about semantic representations of familiarity, since they can be manipulated through experience and biased through sampling.
Manipulating SFDs for target words might be a useful strategy for exploring the degradation of internal
representations of word senses, since the semantic system, given this kind of damage, should find it increasingly more difficult to correctly select the most frequent
word sense of a polysemous word. There is an
increased dependence on contextual information when
performing any lexical-semantic decision task. Without
this context, the patients (and the model) should exhibit increased errors and longer latency responses.

tive.2I Both of these explanations are compatible with the

belief that a reduction in net dopamine levels in the neocortex and other brain areas is responsible for semantic
deficits in patients with PD, which makes it difficult to
decide which explanation is more valid on the basis of
physiological evidence. One way of doing this is to modulate the internal dynamics of the semantic system,
operationalizing a parameter to represent some basic
physiological fact (such as dopaminergic dysfunction).
This idea is not new; Cohen and Servan-Schreiber,"I for
example, used a simple connectionist neural network to
model performance deficits in a lexical decision task in
patients with schizophrenia. Physiological increases in
dopaminergic transmission were operationalized as
increases in gain, with the correct direction of effect in
performance observed. This was taken as evidence for
both the validity of the moderating role of dopamine,
and for the connectionist account of language-processing errors in patients with schizophrenia.
In the semantic system, the word-to-sense-level excitation (a) is computed from the product of the target
word's activation and multiplied by a constant excitation parameter (3). The word-to-sense-level inhibition
(X) is then computed by subtracting the activation for
the target word from the total activation for all words,
and multiplied by a constant (6). Total lateral inhibition
at the sense level () is then computed by:

s=4QxXyz(I) 6

(1)

.1=

where 9 is a word sense inhibition constant. For each word

sense, the lateral sense inhibition ((p) is given by subtracting the product of the activation for the current sense and
the word sense inhibition constant from the total sense lateral inhibition . This partitions the total inhibition at the
word sense level to alternative word senses. Next, the feature-to-sense excitation (K) is computed:
K=VX

Y p(o)

(2)

0=1

Defective processes
As outlined above, an alternative hypothesis to degradation is that the representation of semantic material
(e.g., word senses) is unaffected by the progression of
PD, but that the cognitive processes involved in semantic processing are defective. Specifically, it is thought
that the competitive processes involved in inhibiting
incorrect responses in lexical-semantic tasks are defec-

VTw 4. 24:, n 4, #

where i is the feature output, X is the total number of

features for each word sense, and v is a constant (v). The
feature-to-sense inhibition (x) is then computed by the
product of a constant p, and the difference between the
feature set activation 0 and the total excitation K.
Finally, the net input (a) for each word sense (ignoring
contributions from the phonological route) is given by:
(3)
aX=a+X+(p+K+it
Since 0 is the constant that determines the rate of lat-

.w

Watters ~and,Pate

eral inhibition at the word

lated from

inhibitory

low value

ing

competitive

dopamine

disorders

determining

threshold for

lateral inhibition is

(the

For

correct

epochs,

Fig.

at 38
sense

-0.5, and

3. For

epochs,
of "a

with

with

sense

sense

competition

being

The

-1.0).

select-

clothing;" Fig. 3A).

was

again being

-0.1, the

of

piece

-0.5, the competition

completed

selected

39

at

(Fig. 3B).

For

required

0.8
0.6-

very gross

data

about

0.4-

0.2-

be made. Of interest is

can

deciding just
to observe

responses and increased errors,

ropsychological

ed

-0.1,

shown in

completed

selection that match

sense

neuropsychological

dopaminergic
a

simulate

was

(i.e.,

level

are

with PD. If lateral

patients

about word

from

the lateral

might

available in the neocortex, at

predictions

the

sense

related to the net amount of

negatively

level, predictions

(4)

the

results

processes involved in inhibit-

incorrect responses in

inhibition is

weakly

selection

sense

level

sense

value

modulating

that

inhibition parameter at the

the defective

high

very

be modu-

can

to simulate

strongly inhibitory

hypothesized

It is

system.

-0.1)

selection system, to

to simulate

-1.0)

(4)

level, it

sense
=

as

how much

longer latency

predicted

from

Epochs

neu-

data.

- Snse I -w-Sense 2

Simulations

The winner of the

is defined

for correct

competition

the activation of the word

by

sense

selection

sense

unit that

first reaches the 0.5 activation threshold. The null

0.8
0.6
0.4
0.2

hypothr.

esis is that neither low SFDs

will

anythidng

produce

lateral inhibition

high

nor

but normal semantic

processing

(i.e., degraded representations a-nd defective competitive

processes do not affect correct word
PD-like

errors are

observed

only

inhibition, independently of low

defective

at

or

sense

high

selection). If

high SFDs,

competitive

account for

the errors, without any contribution from

degraded representations. Alternatively,

representations

without

any

els

an

if PD-like

of

defective

from

lateral

possible

Two-sense

0.8

degrad-

0.6

*~0.41

that PD

errors

0.2

arise

high

lev-

inhibition, indicating interdependence

degraded representations

itive processes to

produce

high-SED

PD-like

Epochs

and defective compet-

-Sense 1 -- Sense 2

errors.

words

Fig.

3: Simulations for the

which

example

word BELT is used, which has 2 senses,

with the dominant

sense

of "a

piece

0.23, and the less-dominant

having f

0.07, giving SFD

of

sense

clothing" having
of "deal

0.16. The model

ulated with low, medium and

328

errors

competitive

interaction of both low-SFD words and

between

The

Epochs C

- Snse 1 --Sense 2

alone could account for the errors,

contribution

processes. However, it is also

from

NC'

C~C

observed at any level of lateral inhibition, exclusive-

with low SFD words, this would indicate that

ed

ON

process alone could

ly

V'N

this would

indicate that

were

levels of lateral

high

blow"

was

sim-

lateral inhibition at

has 2

clothing" (f
blow"

(f

0.23),

0.07).

medium and

high

-0.1I

-0.5

(A),

correct

senses

target

and

The

sense

less-dominant

model

was

(B),

and

1.0

of "a

sense

(C).

piece

of "deal

simulated

lateral inhibition at the

sense was

de neuxoscience
Revue &
de psychiatrie
neuroscience
R"ue
h-waiik et de

2-sense, high-SFD word BELT,

dominant

sense

with

of
a

low,

level:

In each case, the

selected.

1 "9
VbLOD 4f
4, 1999
Vol. 24,
24f n0

.~~~~~~~~~~~~~~~~~~~~~~ni proesin

0 = -1.0, the competition was completed at 40 epochs,

with sense 1 again being selected (Fig. 3B). With
increasing lateral sense inhibition, for a system without
degraded representations, the correct word sense is
always selected. Greater lateral inhibition in this case
does not produce PD-like semantic errors, but acts to
produce a pronounced difference in activation between
the target and nontarget word senses, as seen in Fig. 3.
Thus, high lateral inhibition without any degradation of
representation does not produce PD-like errors.

addition, the potential interaction between degraded

representations and defective competitive processes was
examined. The low-SFD word BASS, with the dominant
sense of "fish" having f = 0.16, and the less-dominant
sense of "musical instrument" having f = 0.13, has SFD
= 0.03. BASS was simulated for low, medium and high
A

0.8 0.6 -

Three-sense high-SFD words

0.42-

To ensure that this result is not an artifact of having a

competition between only 2 word senses, a simulation
was performed with a word that has 3 senses: BLUFF has
the different senses of a "ridge" (f = 0.03), a "pretence" (f
= 0.16), and a "gramineous plant" (f = 0.02). This gives
SFD = 0.13, which is high, even though the difference
between the 2 lowest senses is quite low. Thus, if a
degraded representation existed only because the difference between any 2 word senses was small, PD-like processing errors should be observed. The model was simulated with low, medium and high lateral inhibition at the
sense level (i.e., = -0.1, 0 = -0.5, and 0 = -1.0). The
results are shown in Fig. 4. For 0 = -0.1, the correct word
sense was selected after 38 epochs (BLUFF as a "pretence"; Fig. 4A). For 4 = -0.5, the correct word sense was
again selected, after 40 epochs of processing (Fig. 4B). For
0 = -1.0, the correct word sense was again selected, after
42 epochs of processing (Fig. 4C). Thus, with increasing
lateral sense inhibition, for a system without degraded
representations, and for a target word with 3 different
senses, the correct word sense is always selected. Greater
lateral inhibition in this case does not produce PD-like
semantic errors, but acts to produce a pronounced difference in activation between the target and 2 nontarget
word senses, as seen in Fig. 4. This simulation also
demonstrates that, even if the difference between word
sense frequency of nontarget senses is small, this is not
sufficient to produce PD-like semantic processing errors.

Two-sense low-SFD words

Having demonstrated that simply having high lateral
inhibition alone, with a 2-sense or 3-sense word, without
a degraded representation, does not produce PD-like
errors, a final set of simulations was performed to determine the effect of low-SFD words in their own right. In

':

r,
1!. ,-M
..N,.

.:,
1-

PXkno' disease*

Pa

.~02
-n

OCN

ON

Epochs
- Sense 1

Sense 2 -

Sense 3

e .
~ ~

0.8
0.6
0.4

0.20

tON-

(N C
- Cl

ON
Cl

N
CN

Epochs
- Sense 1

Sense 2 -

Sense 3

10.8 uj 0.6 i

0.4

0.2 -

-nclc

Cl

Cl

Epochs
- Sense I

--

Sense 2 -

Sense 3

Fig. 4: Simulations for the 3-sense, high-SFD word BLUFF,

which has 2 senses
a dominant sense of a "pretence"
(f = 0. 16), a "ridge" (f = 0.03), and a "gramineous plant"
(f = 0.02). The model was simulated with low, medium
and high lateral inhibition at the sense level: 0 = -0.1 (A),
0 = -0.5 (B), and = -1.0 (C). In each case, the correct target sense was selected.

Josstnal of .srdiiatty & N

329

.00.imS

Wa:er'a" Pate!

fi: SiA-0S

ii; :-

:;E::ELi4S$t00i0; A0

S0000 00

lateral inhibition at the sense level (i.e., o = -0.1, = -0.5,

and = -1.0), with the results shown in Fig. 5. For =
A

0.6 -

150.4

o e) 0.2-

.1

'0

-_

e-

r-

11

r-

c_

kn

Epochs
-Sense 1 --Sense 2
B

0
_

~ ~

_tN

'I<,

00

0.5
e , 0.2
' 0.1
- c)
t

0-

>l

'-

Epochs
j0.3
C

-Sense I

--- Sense

0.41

<

0.=L
-

GE

r-

t}

0r'

C-

t(,

Epoch

;-Sense 1

"- Sense 2

Fig. 5: Simulations for the 2-sense, low-SFD word BASS,

which has 2 senses
a dominant sense of "a fish" (f =
0. 16), and a less-dominant sense of "musical instrument"
(f = 0.13). The model was simulated with low, medium
and high lateral inhibition at the sense level: = -0.1 (A),
o = -0.5 (B), and v = -1.0 (C). In the case of4) = -0.1, the
incorrect target sense was selected (i.e., a semantic
error), but long latencies were not observed. For = -0.5
= -1.0, both semantic errors and long latencies
and
were observed, suggesting that both degraded representations and defective competitive processes are required
for PD-semantic errors to arise in the model.

33

0000A? AiSftSV

-0.1, the simulation was completed at 39 epochs; however, the incorrect sense of BASS as a "musical instrument" was selected (Fig. 5A). This indicates that simply
having a degraded representation can produce semantic
errors, without any contribution from lateral inhibition.
However, this error does not have the characteristic
increased latency observed in patients with PD; thus,
simply degrading representations without reference to
defective competitive processes is not sufficient to
explain semantic errors in patients with PD. In fact, the
activation profiles for both senses are almost identical,
obviously giving rise to the "confusion" experienced by
the model when attempting to select a correct sense at
the 0.5 activation threshold level.
For = -0.5, the simulation failed to make a selection
by 200 epochs, although the incorrect sense of BASS as
a "musical instrument" received the maximum amount
of activation (Fig. 5B). This indicates that having a
degraded representation (low SFD) can produce PD
semantic errors in combination with a medium level of
lateral inhibition. This demonstrates that both degrading representations and having defective competitive
processes was sufficient to explain observed PD-like
semantic errors. Again, the activation profiles for both
senses were almost identical, however, the 0.5 activation threshold level was not reached. Thus, the model
predicts that, without the provision of context, a patient
with PD would make errors approximately 50% of the
time if forced to make a response after long latency.
For = -1.0, the simulation again failed to make a
selection by 200 epochs, with neither word sense reaching the 0.5 activation level (Fig. 5C). The peak level of
action reached (0.32) was identical for both word senses, and so the selection of a correct word sense was
clearly impossible under these conditions. This again
indicates that having a degraded representation (low
SFD) can produce PD-like semantic errors in combination with a high level of lateral inhibition, suggesting
that both an interaction between degraded representations and defective competitive processes is the most
plausible explanation for the observed semantic errors.
Again, the model predicts that, without the provision of
context, a patient with PD would make errors approximately 50% of the time if forced to make a response
after the long latency observed in this simulation.

Discussion
The results of this study demonstrate

de pq.l
psychiatrie
kevu &
I.w uw.,etft. ;.de 1-4,ueuroscience
io-iitt ience
10

.Revue

:4

one way

in which

Vol
24,4777">.,0ifw:0
n" 4, 19W
W0`

::f

PD-like semantic errors can arise in a semantic system.

From the results presented above, neither degraded representations nor defective competitive processes alone
were sufficient to account for both the increased errors
and longer latencies for PD-like semantic deficits. High
levels of word sense lateral inhibition had no effect on
representations with a high SFD, indicating that a degraded representation was necessary for any effect of a defective competitive process to appear. Conversely, although
errors did occur for low-SFD words at low levels of lateral inhibition, these did not exhibit the long latencies characteristic of patients with PD. In fact, long-latency errors
only appeared at high levels of lateral inhibition for lowSFD words. This suggests that degraded representations
were responsible for the error in sense selection, but that
defective competitive processes were responsible for the
increased latency observed in PD errors. Neither degraded representations nor defective competitive processes
alone, in their own right, were sufficient to reproduce
symptoms of PD. However, an interaction between the 2
components was observed, suggesting a general mechanism for the "semantic deficit" of patients with PD.
This model has made many simplifying assumptions
about the structure and dynamics of the nervous system.
However, it suggests an explanation for understanding
semantic processing deficits in patients with PD which
has not been previously suggested (i.e., that an interaction between degraded representations and defective
competitive processes is required for PD semantic processing errors to appear). This indicates a possible reconciliation between the views of McDonald et al2 and
Gurd and Oliveira,2' in order to develop an integrated
view of semantic processing deficits in patients with PD.
Clearly, the results of this study provide 2 general
mechanisms by which semantic errors can arise. But are
these predictions sufficiently specific to usefully understand PD language behaviour and dopaminergic neuroscience? Further studies must take 3 paths in order to
answer this question. First, the general relation between
net dopamine levels in the neocortex (which are
reduced in patients with PD) and the actual dynamics
of dopamine transmission in specific brain areas, needs
to be further developed in a reductionist way. Since this
study has identified some general nonlinear activation
processes that successfully model aspects of normal
verbal behaviour and abnormal PD-like symptoms, it is
important to further develop more specific dopaminergic models that can replace the simple constant rates of
activation presented in equations 1 and 2. Fortunately,

Vol.
4,..i:i.
1999
VW
h.i.
N224,
i~ no A
:EEI
^i.

*'

.i ~

0'

L0

SR

tALdt: ttt

00t4

Semantic prc ssn in Park inson' diseas

--:

the modular structure of the semantic system presented

in this study can accommodate this kind of substitution.
Second, testing the semantic system in isolation does not
account for the activity in the nonsemantic lexical route in
normal reading and language processes, or the activity of
the nonlexical route. It is possible that the results presented here may only exist when there is a disturbance in
process or representation, or when the semantic system is
simulated in isolation from the rest of the model. The present simulations do not account for situations in which
meanings are learned through regularization in the nonlexical route, so only learned words (and not pronounceable nonwords, for example) are now being tested. Future
studies need to examine the dynamic interaction between
the semantic system and other routes to cognition and
reading, particularly in the context of semantic priming.
Such generalizations are necessary in order to understand
how the processing of at least 2 words (and possibly whole
phrases) in succession could give rise to semantic judgement errors in patients with PD, under the low-SFD conditions described in this paper.
Finally, studies must be undertaken to determine
whether it is possible to simulate other behavioural conditions, which might be important in reducing semantic
deficits in patients with PD (i.e., to predict a useful clinical intervention). For example, if patients with PD exhibit a strong dependence on context, could some context be
presented to the model, in the form of semantic priming,
to estimate how much context is required for successful
semantic processing? Under the condition of degraded
representations and high word sense lateral inhibition, it
should be possible to present a prime word related to a
single sense of the target word, to determine the minimum stimulus onset asynchrony required to elicit a correct response in a lexical processing task. Priming would
need to occur at the semantic feature level, as described
in this model, since the similarity between word senses of
the target and prime words are defined by their possession of common semantic features, which could accrue
net feature activation. This would demonstrate not only
that the model has some vague usefulness in understanding some of the cognitive processes involved in
producing semantic deficits in patients with PD, but also
that it could actually make useful empirical predictions
that might assist the planning of clinical interventions.

Acknowledgements
We would like to acknowledge informative discussions

Jotzrnal oi Psychiatry & Neus.oscience

.0i

33,

at
IIII1:
i,

Watters and Patel

with Professor Max Coltheart (Macquarie University,

Australia) and Dr. Jennifer Gurd (Oxford University,
UK) during the preparation of this manuscript. This
research was generously supported by a grant from the
Australian Research Council (ARC).

References
1.
2.
3.
4.

5.
6.

7.
8.
9.

10.
11.

12.
13.
14.

15.
16.

17.

332

Hornykiewicz 0. Biochemical aspects of Parkinson's disease.

Neurology 1998;51(2 Suppl): S2-9.
Zimmermann R, Deuschl G, Hornig A, Schulte-Monting J,
Fuchs G, Lucking C. Tremors in Parkinson's disease: symptom
analysis and rating. Clin Neuropharmacol 1994;17:303-14.
Brod M, Mendelsohn GA, Roberts B. Patients' experiences of
Parkinson's disease. J Gerontol B Psychol Sci Soc Sci
1998;53(4):213-21.
Javoy-Agid F, Agid Y. Is the mesocortical dopaminergic system
involved In Parkinson's disease? Neurology 1980;30:1326-30.
Braak H, Braak E, Yilmazer D, de Vos RA, Jansen EN, Bohl J.
Pattern of brain destruction in Parkinson's and Alzheimer's
diseases. J Neural Transm 1996;103:455-90.
Robbins T. Cognitive deficits in schizophrenia and Parkinson's
Disease: neural basis and the role of dopamine. In: Willner P,
Scheel-Kurger J, editors. The mesolimbic dopamine system: from
motivation to action. Chichester: Wiley; 1991.
Levita E, Riklan M, Cooper I. Psychological comparison of unilateral and bilateral thalamic surgery: a preliminary report. J
Abnorm Psychol 1967;72: 251-4.
Hammen VL, Yorkston KM. Speech and pause characteristics
following speech rate reduction in hypokinetic dysarthria. J
Commun Disord 1996;29:429-44.
Illes J, Metter EJ, Hanson W, Iritani S. Language production in
Parkinson's disease: acoustic and linguistic considerations.
Brain Lang 1988;33:146-60.
Small JA, Lyons K, Kemper S. Grammatical abilities in
Parkinson's disease: evidence from written sentences.
Neuropsychologia 1997;35:1571-6.
Geyer HL, Grossman M. Investigating the basis for the sentence comprehension deficit in Parkinson's Disease. J
Neurolinguistics 1994;8:191-205.
Gurd JM, Bessell N, Watson I, Coleman J. Motor speech versus
digit control in Parkinson's disease: a cognitive neuropsychology investigation. Clin Linguistics Phonetics In press.
Watters PA, Gurd JM. A review of cognitive and neurolinguistic deficits in Parkinson's disease. South Pacific J Psychol
1998;10:112-9.
Cohen H, Bouchard S, Scherzer P, Whitaker H. Language and
verbal reasoning in Parkinson's disease. Neuropsychiatry
Neuropsychol Behav Neurol 1994;7:166-75.
Gurd JM. Frontal dissociations: evidence from Parkinson's disease. J Neurolinguistics 1995;9:55-68.
Beatty W, Monson N. Lexical processing in Parkinson's disease
and multiple sclerosis. J Geriatr Psychiatry Neurol 1989;2:145-52.
Illes J. Neurolinguistic features of spontaneous language production dissociate three forms of neurodegenerative disease:
Alzheimer's, Huntington's, and Parkinson's. Brain Lang
1989;37:628-42.

Revue de

18. Gurd JM. Word search in patients with Parkinson's disease. I

Neurolinguistics 1996;10:207-18.
19. Spicer KB, Brown GG, Gorell J. Lexical decision in Parkinson
disease: lack of evidence for generalized bradyphrenia. J Clin
Exp Neuropsychol 1994;16:457-71.
20. van Spaendonck KP, Berger HJ, Horstink MW, Borm GF, Cools
AR.. Memory performance under varying cueing conditions in
patients with Parkinson's disease. Neuropsychologia
1996;34:1159-64.
21. Gurd JM, Oliveira RM. Competitive inhibition models of lexical-semantic processing: experimental evidence. Brain Lang
1996;54:414-33.
22. McDonald C, Brown G, Gorell J. Impaired set-shifting in
Parkinson's disease: New evidence from a lexical decision task.
J Clin Exp Neuropsychol 1996;18:793-809.
23. Auriacombe S, Grossman M, Carvell S, Gollomp S, Stern M,
Hurtig H. Verbal fluency deficits in Parkinson's disease.
Neuropsychology 1993;7:182-92.
24. Miyata Y, Tachibana H, Sugita M. Memory function in aging
and Parkinson's disease-an event-related potential study.
Nippon Ronen Igakkai Zasshi 1998;35:464-71.
25. Leplow B, Dierks C, Herrmann P, Pieper N, Annecke R, Ulm G.
Remote memory in Parkinson's disease and senile dementia.
Neuropsychologia 1997;35:547-57.
26. Galletly CA, Clark, CR, McFarlane, AC. Artificial neural networks: a prospective tool for the analysis of psychiatric disorders. J Psychiatry Neurosci 1996;21:239-47.
27. Devitt M. Realism and truth. London: Blackwell; 1991.
28. Barlow HB. Single units and sensation: a neurone doctrine for
perceptual psychology? Perception 1972;1:371-94.
29. Putnam H. The meaning of "meaning." In: Gunderson K, editor. Language, mind and knozvledge. Minneapolis: University of
Minnesota Press; 1975.
30. Coltheart M, Curtis B, Atkins P, Haller, M. Models of reading
aloud: dual-route and parallel-distributed-processing
approaches. Psychol Rev 1993;100:589-608.
31. Patel M. Using neural nets to investigate lexical analysis. In:
Foo N, Goebel R, editors. Lecture notes in artifical intelligence. no.
1114. Berlin: Springer; 1996.
32. Watters PA. Cognitive theory and neural model: the role of
local representation [comment]. Psycoloquy 1998;9:20. Comment on: Green CD. Are connectionist models theories of cognition? Psycoloquy 1998;9(4).
33. Miller GA, Beckwith R, Fellbaum C, Gross D, Miller KJ.
Introduction to WordNet: an on-line lexical database. Int J
Lexicography 1990;3:235-44.
34. Collins AM, Quillan MR. Retrieval time from semantix memory. J Verbal Learning Verbal Behav 1969;8:240-7.
35. Wilkins A. Conjoint frequency, category size, and categorisation time. J Verbal Learning Verbal Behav 1971;10:382-5.
36. Twilley LC, Dixon D, Taylor D, Clark K. University of norms of
relative meaning frequency for 566 homographs. Mem Cognit
1994;22:111-26.
37. Watters PA, Patel M. A neural network model of semantic processing errors in Parkinson's disease. Neural Proc Lett 1998;9:1-11.
38. Cohen JD, Servan-Schreiber D. Context, cortex and dopamine:
a connectionist approach to behavior and biology in schizophrenia. Psychol Rev 1992;99:45-77.

psyhine et de neuroscience

VL. 24, n0 4,. 1999