Frontal Cognitive Function and Memory in Parkinson’s Disease: Toward a Distinction between Prospective and Declarative Memory Impairments?
Frontal cognitive function and m e m o r y in Parkinson's disease: toward a distinction between prospective and d e c l a r a t i v e m e m o r y impairments?
. Trester 0 1
J.A. Fields 0 1
0 Center , 3901 Rainbow Boulevard, Kansas City, KS 66160-7314 , USA
1 Department of Neurology, University of Kansas Medical Center , Kansas City, KS , USA
Memory dysfunction is a frequent concomitant of Parkinson's disease (PD). Historically, two classes of hypotheses, focusing on different cognitive mechanisms, have been advanced to explain this memory impairment: one postulating retrieval deficits (common to several neurodegenerative disorders involving the basal ganglia), and the other postulating frontally mediated executive deficits as fundamental to memory impairment. After outlining empirical support for the retrieval deficit hypothesis, research on the more recent "frontal executive deficit hypothesis" is reviewed, and major challenges to this hypothesis are identified. It is concluded that the frontal executive deficit hypothesis cannot adequately account for all memory impairments in PD, and that a more parsimonious theoretical account might invoke a distinction between prospective and declarative memory impairments. It is suggested that there may be three subgroups of PD patients: one demonstrating prospective memory dysfunction only, one with declarative memory dysfunction only, and one with both prospective and declarative memory dysfunction. Consequently, PD might provide a useful model within which to investigate the relationship between prospective and declarative memory.
Dementia - Executive functions - Frontal lobes - Memory - Parkinson's disease
Memory impairments are acknowledged to be
among the most common cognitive deficits in Par
(PD; Beatty 1992a,b)
but the phe
nomenology, and the cognitive and neural underpin
nings of such memory impairments remain poorly
understood. Current hypotheses about the cognitive
mechanisms underlying PD memory dysfunction fall
into two broad categories: one postulating a failure
in retrieval operations associated with basal ganglia
pathology, and the other postulating an impairment
of executive functions (e.g. self-initiated strategic in
formation processing) associated with frontal and/ or
frontostriatal pathology. Some
(e.g. Dubois et al.,
see these hypotheses as related, thus propos
ing that retrieval deficits in PD reflect an executive
deficit. However, there is a subtle distinction be
tween the "frontal executive" and "subcortical re
trieval" interpretations of PD memory impairment.
Whereas the traditional retrieval deficit hypothesis
suggests that PD compromises access to stored mem
ories, the frontal hypothesis proposes that the strate
gies required to initiate and/or maintain efficient
retrieval and other cognitive operations are
One difficulty faced when studying memory in PD
is that PD-associated cognitive impairment is rather
variable. Indeed, in an attempt to bestow order upon,
and understand conflicting empirical findings concern
ing cognitive impairment in PD, several authors have
advocated subgrouping PD on the basis of cognitive
impairment patterns. For example,
Dubois et al.
proposed that there are three subgroups of
PD patients: those with dementia, those with circum
scribed cognitive deficits, and those who are cogni
tively intact. Certainly, most investigators agree that
only a subset of PD patients develop dementia, with
prevalence estimates ranging from 20% to 30%
(Mohr et al., 1995)
. Because much of our understand
ing of the cognitive and rieural mechanisms under
lying impaired memory in PD has come from the
fruitful application of experimental cognitive psycho
logical paradigms to clinical neuropsychological stud
ies of dementia
(see Butters 1984, 1992)
, a brief
historical overview of the rise and decline of the
"cortical vs subcortical" dementia distinction high
lights the evolution of the explanations for memory
impairment in PD.
At the outset, it must be stated that this paper
concerns itself only with declarative memory, to
which the retrieval deficit and executive dysfunction
hypotheses are applicable. Readers interested in how
neuropsychological studies of PD have informed the
distinction between declarative and non-declarative
are referred to Butters et al.
Soliveri et al. (1992)
for recent reviews.
A brief historical perspective on the "cortical subcortical" dementia distinction: emergence of the retrieval deficit and executive dysfunction hypotheses
Dementia was initially thought of as a unitary behav
ioral syndrome, characterized by a homogeneous de
cline in intellectual functions, regardless of etiology.
Subsequently, programmatic studies of cognition in
dementias yielded data suggesting that the pattern of
cognitive dysfunction in dementia was heterogeneous,
depending largely upon whether the pathological
process affected predominantly cortical or subcortical
structures. Consequently, a distinction was drawn
between "cortical vs subcortical" dementias
mings and Benson, 1984)
. Although the term "subcor
tical dementia" was first used by Albert et al. (1974)
to refer to the cognitive impairment in progressive
supranuclear palsy, the term subsequently came to
refer to a variety of dementias associated primarily
with subcortical pathology early in the course of
these diseases [e.g. PD, Huntington's disease (HD)
and mUltiple sclerosis (MS)], which were thought to
lead to similar patterns of cognitive impairment.
Generally, the quality of memory impairment in
PD parallels that observed in other "subcortical"
dementias, but is readily contrasted to the nature of
memory impairments in Alzheimer's disease (AD),
the prototypical "cortical" dementia. First, PD pa
tients typically demonstrate impaired recall for verbal
material such as word lists, prose passages and paired
associates, but their recognition of the same material
is only slightly, if at all, impaired
(Huber et ai.,
1986a; Helkala et ai., 1988; Beatty et ai., 1989a;
Levin et ai., 1989; Mohr et ai., 1990; Bondi and
Kaszniak, 1991; Pillon et ai., 1993; Breen, 1993;
Buytenhuijs et ai., 1994; Cohen et ai., 1994; Tsai et
. This performance pattern stands in con
trast to the impaired recall and recognition observed
(Heindel et ai., 1993; Pillon et ai., 1993; Bondi
et ai., 1994)
. Second, PD patients without significant
cognitive impairment have relatively normal rates of
forgetting, and tend not to commit a large number of
intrusion errors (an index of heightened sensitivity to
proactive interference). Although PD patients with
dementia show more rapid rates of forgetting and
commit more intrusion errors than do PD patients
without dementia, these abnormalities are still not as
pronounced as in AD when the groups' overall sever
ity of dementia is comparable
(Beatty et ai., 1989b;
Kramer et al., 1989; Massman et ai., 1990; Pillon et
ai., 1993; Stem et ai., 1993)
. In addition, whereas the
remote memory loss in AD is characterized by a
temporal gradient (with relative preservation of more
distant memories), retrograde amnesia in PD, like
HD, is equally severe for all past decades
ai., 1988; Freedman et ai., 1984; Huber et ai., 1986b,
but see Sagar et ai., 1988a)
. Together, these findings
have been interpreted as supporting the hypothesis
that memory impairment in PD is primarily a func
tion of retrieval deficits, a mechanism thought
common to several "subcortical" dementias. That
retrieval deficits underlie recall impairments in PD
has also been supported by the finding that non-PD
patients with focal basal ganglia lesions show im
paired recall but intact recognition memory (Dubois
et ai., 1995). In contrast, memory impairment in
"cortical" dementias such as AD is thought to reflect
disturbed encoding, consolidation, and storage of
Held untenable on neuroanatomical grounds be
cause most dementias eventually compromise both
cortical and subcortical structures
(Boller et ai., 1980;
, the distinction between "cortical"
and "subcortical" dementia nonetheless persisted
and was defended on the basis of its clinical utility
(Cummings, 1986, 1988a)
, and neuropsychological
evidence highlighting the heterogeneity of cognitive
impairments associated with early "cortical" (AD)
and "subcortical" (PD and HD) dementias. More
detailed and sophisticated neuropsychological studies
of the different dementias, as advocated by Brown
and Marsden (1988), have, however, revealed that
etiologically distinct "subcortical" dementia cognitive
impairment patterns are as dissimilar as they are
similar. Thus, although the "cortical-subcortical" dis
tinction may have broad heuristic value
(Dubois et ai.,
, several authors have advocated as preferable
an investigative strategy relating specific cognitive
impairments to specific diseases
(Pillon et al., 1991;
Heindel et ai., 1993)
. Indeed, research into disease
specific cognitive impairment has led to the formula
tion of increasingly refined and detailed hypotheses
about the nature of memory impairment in PD, both
with and without dementia. Specifically, the notion
that retrieval deficits underlie impaired memory in
PD, and consequently that there is a primary memory
impairment in PD, was widely accepted. More re
cently, some authors have questioned whether
memory impairment in PD is a "true" memory im
pairment. Instead, these authors have proposed that
memory impairment is a feature secondary to execu
tive deficits (e.g. an inability to generate efficient
strategies demanded by tasks involving self-initiated
planning) associated with frontal dysfunction
Taylor et al., 1990; Pillon et al., 1993)
Albert suggested in 1978
that the term "frontosub
cortical" dementia rather than "subcortical" demen
tia might more appropriately describe cognitive
impairments in subcortical diseases, but the possibil
ity that frontal or frontostriatal (as opposed to purely
striatal) dysfunction underlies PD memory deficits
did not receive serious consideration until this pro
posal was specifically advanced by
Taylor et al.
. Given that PD patients have been consistently
shown to have a variety of executive deficits
et al., 1990; Cronin-Golomb et al., 1994; Levin and
, and given that many cognitive (includ
ing memory) tasks "rely on one or more executive
(Levin and Katzen, 1995)
, one might
accept Taylor et al.'s (1986) proposal as at least face
valid. We now turn to review subsequent research
into the role of frontal cognitive functions in PD
memory impairment which highlights that the issue
of the relationship between frontal cognitive and
memory functions in PD is considerably more conten
tious. The debate about the relative merits of the
retrieval and executive deficit hypotheses, and about
the neural basis of PD memory impairment is unlikely
to be resolved soon because, to some extent, this
debate parallels the continuing controversy about
whether the frontal lobes serve a primary function in
(see Schacter, 1987; Shimamura et al., 1991;
STUDIES OF THE ROLE OF FRONTAL
COGNITIVE FUNCTIONS IN PD MEMORY
Recent research into the role of frontally mediated
cognitive mechanisms in PD memory impairment
can be broadly conceived as following four strategies
of investigation: (1) the elucidation of the qualitative
nature of memory impairment in PD, and its extant
comparison to that reported in studies of patients
with frontal lesions; (2) correlation of scores on
memory tests and neuropsychological measures pur
portedly sensitive to frontal dysfunction; (3) the study
ofPD patients' performance on memory tasks report
edly impacted specifically by frontal dysfunction; and
(4) elucidation of the relationship between memory
test performance on one hand, and regional cerebral
blood flow, glucose metabolism and [isF]-dopa
uptake determined via functional neuroimaging, on
the other hand. Results from studies in each of the
above categories are reviewed below.
Qualitative parameters of PD memory impairment
In their influential paper,
Taylor et al. (1986)
that although their PD sample's memory was "gener
ally intact", deficits were observed on immediate
recall of two prose passages, on a spatial delayed
recognition task (DRT), and on the Rey Auditory
Verbal Learning Test
(RAVLT; Rey, 1964)
, a word
list learning and memory test.
Taylor et al. (1986)
explained impaired immediate but intact delayed
recall of the prose passages in terms of slowed infor
mation processing (consistent 'with frontostriatal dys
function), but intact encoding, storage and retrieval.
Although they did not suggest a cognitive mecha
Taylor et al. (1986)
excluded temporal lobe
mediated mechanisms as accounting for impaired
immediate recall on the RAVLT word list by stating
that the intact primacy effects observed in PD are
not observed in patients with hippocampal damage.
Taylor et al. (1986)
found that the nature of
the PD group's impairment on the Wisconsin Card
(WCST; Heaton, 1981)
, an executive
function test requiring conceptualization of card sort
ing rules and modification of response strategy to
verbal feedback, was typical of that observed in fron
tal lesion patients. The most parsimonious explana
tion of the sum of these findings, according to
et al. (1986)
, is that frontal dysfunction in PD compro
mises the ability to generate efficient strategies on
tasks requiring self-initiated planning.
Several challenges confront Taylor et al.'s (1986)
"frontal dysfunction" explanation of PD memory
Taylor et al. (1986)
pointed out that a normal primacy effect in PD
makes it unlikely that temporal lobe dysfunction
underlies the PD group's immediate recall impair
ment on the RAVLT. However, their finding of a
normal recency effect is not supportive of the "frontal
dysfunction" explanation offered because diminished
recency effects have frequently been observed in
patients with frontal lesions
(see Eslinger and Grattan,
. Equally plausible would be the traditional
retrieval deficit (associated with basal ganglia pathol
ogy) hypothesis given their finding of impaired im
mediate recall but intact recognition of the word list.
Second, Beatty et al. (1989a), although also finding
early PD patients to be impaired on the WCST, did
not find the errors to be consistent with those made
by frontal lobe patients. Thus, the possibility is raised
that impairments observed by
Taylor et al. (1986)
the WCST and memory tasks were related by virtue
of their correlation with another variable. Indeed,
Taylor et al. (1986)
conceded that relationships ob
served between WCST and RAVLT, and between
DRT and RAVLT scores, might be accounted for by
correlations between these variables and a third vari
able (e.g. intelligence or disease severity).
Taylor et ai.'s (1986) notion that a frontally medi
ated impairment in the ability to generate efficient
strategies is at the root of PD memory impairments
has been supported by several authors' finding that
PO patients inefficiently use a semantic clustering
strategy during encoding of word lists
ai., 1990; Taylor et ai., 1990; Karamat et ai., 1991;
Buytenhuijs et ai., 1994)
. Whether inefficient semantic
encoding is necessarily a consequence of frontal dys
function is questionable, however. For example,
Janowsky et al. (1989a) observed normal release from
proactive interference (for which semantic encoding
is a prerequisite) in patients with frontal lobe lesions,
Freedman and Cermak (1986)
found that seman
tic encoding was not deficient in all patients with
bilateral frontal lobe disease. Furthermore, Beattyet
al. (1989b) found that PO patients' poor performance
on a semantic verbal fluency test was more related to
performance on other measures of semantic memory
access than to executive function measures. This
raises the possibility that inefficient use of semantic
encoding strategies reflects an impairment in semantic
memory access rather than a difficulty initiating effi
Another challenge to the frontal cognitive dysfunc
tion hypothesis is that executive and memory impair
ments are dissociable in at least some groups of PD
patients. Specifically, PD patients have been observed
to have memory impairments in the absence of execu
(e.g. Mohr et al., 1990)
dysfunction but not declarative memory impairments
(Owen et al., 1992). Among unmedicated mild, and
medicated mild and moderate PD groups,
found that attentional set-shifting was im
paired in all three groups of patients but that none of
these groups was impaired on pattern recognition.
Furthermore, although the medicated mild PD group
Owen et al. (1992)
study was impaired on a
spatial working memory task [a finding contrary to
that reported by
Morris et al. (1988)
using a different
form of the task], the group was not impaired on
visual pattern or spatial recognition, non-verbal
paired associated learning, or immediate and delayed
matching to sample tasks. Given Owen et al.'s (1995a)
finding that these spatial working memory and spatial
recognition tasks are more sensitive to frontal than
temporal lobe damage, whereas pattern recognition
and delayed matching to sample are more sensitive
to temporal damage, it is likely that memory func
tions mediated by the temporal, but not frontal lobes,
are relatively preserved in early PD.
In addition to demonstrating the dissociability of
executive and memory impairments in PD,
also observed some important differences
in the quality of some of the executive deficits shown
by the PD patients and by frontal lesion patients in
(Owen et at., 1990, 1991)
. On the
Tower of London problem, medicated PD patients
demonstrated slowed initial planning time, but
normal subsequent thinking time (i.e. time for plan
ning moves after the first move). The converse was
observed in frontal lesion patients. In other words,
these patients were normal in planning time for the
initial move, but slow in planning subsequent moves.
Furthermore, the diminished solution accuracy ob
served in the frontal patients was only noted among
more severe PD patients taking medications.
Although studies of the quality of memory impair
ment in PD may inform about similarities and dis
similarities between memory impairments in PO and
frontal patients, a major difficulty of these studies is
that they generally fail to establish a relationship be
tween the memory impairment and frontally mediated
executive deficits. Obviously, the demonstration of a
correlation between memory impairments and other
executive deficits would provide stronger evidence
that the memory impairment is indeed related to
frontal cognitive dysfunction. In pursuit of this aim,
several studies have evaluated the relationship be
tween scores on memory tests and neuropsychological
tests of "frontal cognitive functions" (e.g. the WCST).
Relationship between performance on memory and "frontal cognitive function" tasks
Bondi et al. (1993)
found that the memory and
visuospatial test performances of non-demented PD
patients no longer differed from those of elderly
controls once scores on a series of "frontal lobe tests"
, California Sorting
(Delis et al., 1992)
, verbal fluency, and a verbal
temporal ordering task
(after Sagar et al., 1988b)
were covaried. However, the converse was not true.
That is, PD patients' performance on the frontal
tests was still inferior to that of controls even when
memory and visuoperceptual test performance was
covaried. Bondi et al. (1993) interpreted these find
ings as supportive of the frontal dysfunction hypoth
esis of cognitive impairment in PO. Bondi et al.'s
(1993) study is elegant in that it is the only
correlational study to date that has included the critical step
of examining both the effects of executive function
on memory, and of memory on executive function in
PD. Univariate analyses carried out by these authors
to supplement multivariate analyses raise an interest
ing issue, however. Specifically, whereas PD and con
trol groups differed significantly in their performance
on each of the four frontal tasks, they differed on
only one of four memory tasks. Consequently, the
results of the multivariate analyses of covariance are
not surprising. If PD and control groups demon
strated little difference in memory to begin with (i.e.
PD patients did not have a convincing memory im
pairment), statistical covariance of frontal measure
scores is apt to eliminate this minimal difference.
Cooper and Sagar's (1993)
findings might also be
interpreted as not particularly supportive of the fron
tal cognitive dysfunction hypothesis of PD memory
Cooper and Sagar (1993)
PD patients to be impaired in the recall of objects
but not their spatial locations. Because the frontal
lobes are known to have an important role in the
processing of spatial context
(Grattan and Enslinger,
, and because frontal lesion patients have been
shown to demonstrate deficits on spatial recognition
and working memory tasks
(e.g. Owen et al., 1995a)
Cooper and Sagar's (1993)
finding of intact spatial
location recall (together with impaired object recall
which might reflect temporal dysfunction) might be
taken not to support the executive dysfunction hy
pothesis of PD memory impairment. Second, in the
Cooper and Sagar (1993)
study, item recall correlated
significantly with only WCST perseverative responses
(r = - 0.25), but not categories achieved or trials to
first category. Thus, even though number of perse
verative responses is the WCST index most sensitive
to frontal dysfunction, it shared only about 6% of
variance with item recall. Furthermore, item recall
correlated significantly with a measure of overall
severity of cognitive impairment [Blessed Dementia
Scale (BDS; Blessed et al., 1986) score] (r = - 0.53),
age (r = - 0.40), New Adult Reading Test
Nelson and O'Connell, 1978)
score (r = 0.28),
Wechsler Memory Scale (WMS; Wechsler, 1945)
Memory Quotient (MQ) (r = 0.65) in addition to
(Cooper et al., 1991)
(r = 0.67) and
(Brown, 1958; Peterson and Pe
score (r = - 0.40). Because multiple
regression analyses were not reported, it is difficult
to assess the unique contribution of executive func
tion variables to impaired item recall, but it appears
that item recall may be just as, or more strongly
related to performance on tests not traditionally con
sidered frontal cognitive function tests.
PD patients' performance on two word list memory
tests was found by
Pillon et al. (1993)
to be highly
related to scores on four executive function tests
[WCST categories achieved, Dementia Rating Scale
(DRS; Mattis, 1988)
semantic verbal fluency, and phonemic verbal flu
ency] and to a "frontal" score based on behavioral
abnormalities. Although supportive of the "frontal
hypothesis" of memory dysfunction in PD, several
concerns remain. First, the correlation between
memory and frontal test scores may reflect the rela
tionship each of these variables bears to a third
variable (e.g. severity of overall cognitive impair
ment). This is suggested by the fact that in Pillon et
al.'s (1993) study, memory, executive function and
linguistic test scores loaded on one factor accounting
for 80% of the variance. Second, significant correla
tions between executive function test scores and those
memory test scores typically assumed to be sensitive
to frontal dysfunction were not reported. For exam
ple, for the CVLT, correlations (ranging from 0.54 to
0.77) were reported between immediate recall, long
delay cued and free recall, and semantic clustering on
the one hand, and WCST, DRS Initiation scale,
phonemic fluency, category fluency and "frontal
score" on the other hand. No significant correlations
were reported between "executive function" scores
and CVLT intrusions, perseverations, the contrast
between List A and B recall (a measure of proactive
interference), and primacy and recency region scores.
Finally, a recent study of the construct validity of
the WCST in PD
(Paolo et al., 1995)
performance on memory tests such as the Continuous
Visual Memory Test
(CVMT; Trahan and Larrabee,
, the CVLT, and the WMS-R Logical Memory
subtest might be relatively independent of WCST
performance. Specifically, among both normal elderly
and individuals with PD, WCST scores loaded on a
factor separate from one on which the memory test
In summary, the studies relating memory and "fron
tal" test performances provide only weak support for
the frontal cognitive dysfunction hypothesis of
memory dysfunction in PD. Specifically, modest cor
relation coefficients between executive and memory
test scores indicate that only a small proportion of
variance in these scores is shared. Although these
studies provide a first step in testing the frontal
hypothesis by using rather global measures of
memory and executive functions, they do not estab
lish whether a relationship exists in PD between
"frontal" test scores and memory variables thought
to be specifically related to frontal lobe function.
Several studies have been carried out to examine PD
patients' performance on memory tasks known to be
impacted specifically by frontal dysfunction.
Performance of PO patients on "frontal" memory tests
Several studies employing experimental paradigms
indicate that patients with frontal lobe lesions may
experience deficits in highly specific aspects of
memory. One type of memory in which the frontal
lobes appear to playa critical role is that for temporal
(Milner et al., 1985; Hambrecht, 1987;
Schacter, 1987; Petrides, 1989)
. Such deficits in tempo
ral order memory have been suggested as the basic
mechanism underlying frontal lobe patients' impair
ments in recency discrimination
(Milner et al., 1985;
McAndrews and Milner, 1991; Butters et al., 1994;
Eslinger and Grattan, 1994)
and source memory
. Consequently, several authors seek
ing to determine whether PO memory impairment is
related to frontal dysfunction have examined PO
patients' performance on a range of memory tasks
sensitive to frontal dysfunction, including recency
discrimination, delayed response and alternation,
source memory, subject-ordered tasks, and condi
tional associative learning. Studies of PO using each
of these paradigms are reviewed below.
Recency discrimination. Sagar et al. (1988a) found
that PO patients' recognition of events in remote
memory was relatively intact, but that they had diffi
culty dating these same events. It is thus possible that
poor temporal memory / recency discrimination or se
quencing affects PO patients' ability to date, but not
to recall, events in remote memory.
inferred from PD patient's impaired
recency discrimination, but intact content recognition
of verbal and non-verbal stimuli, that disordered
temporal memory also impacts performance on an
terograde memory tests.
Fischer et al. (1990)
found poor recency recognition in PO. Although
these authors ascribed the disordered temporal
memory to possible frontal dysfunction, they did
not correlate performance on memory and frontal
cognitive function tests.
In a subsequent study,
Cooper et al. (1993)
report correlations among temporal memory and
frontal cognitive function test scores. Specifically,
Cooper et al. (1993)
investigated temporal memory
in PO by examining content recognition and recency
discrimination using a modification of Sagar et al.'s
(1988b) verbal temporal ordering task. Two of their
findings are of particular note. First, although PO
patients made more errors on the task overall than did
controls, there was no disproportionate impairment
in recency discrimination relative to content recogni
tion. On the task as a whole, content recognition
correlated only with age, whereas recency discrimi
nation correlated significantly with digit ordering
(r = 0.23), WCST categories (r = 0.36) and BDS
(r = - 0.20). Second, when recency discrimination
was analyzed as a function of stimulus-test interval,
an impairment was observed in recency discrimina
tion, but not content recognition, at the shortest
stimulus-test interval. Recency judgement at the two
shortest intervals in PO correlated significantly with
scores on two WCST variables [number of categories
(r = 0.29 to 0.40) and trials to first category (r =
0.27 to - 0.40)], a digit ordering task (r = 0.33 to
0.52), the Brown-Peterson task (r = 0.41 to 0.45),
WMS MQ (r = 0.32 to 0.47) and BOS (r = - 0.24
to - 0.35). The effect sizes associated with these
correlation coefficients are modest, and likely repre
sent overestimates given the probable intercorrela
tions among measures. Thus, although the findings
Cooper et al. (1993)
clearly point to the independ
ence of recency and content recognition, the extent
of the association between recency discrimination
and frontal cognitive functions is difficult to deter
mine, but likely small.
Delayed response and delayed alternation.
Two spatial delayed response tasks apparently are
highly sensitive to prefrontal pathology
and Oscar-Berman, 1986a)
, and are thought to
depend on temporal memory (Oscar-Berman, 1991).
Delayed response (DR) tasks involve a reward being
placed under one of two or more identical stimuli (in
different locations) in full view of the subject. As
soon as the stimuli cover the reward, a screen is
placed between the subject and the stimuli. Following
a brief interval, the screen is raised and the subject
has the opportunity to move one of the stimuli.
Obviously, if, and only if, the correct choice is made,
the subject receives the reward under the stimulus.
The OR task thus has a temporal dimension since
the subject must delay a response until given the
opportunity to respond. The delayed alternation
(DA) task is similar to DR in terms of apparatus
employed, but different in that the task is both time
based and response-patterned by virtue of the alterna
tion of stimulus-outcome across trials. Whereas
damage to the ventral prefrontal system impairs pre
dominantly DA performance, damage to the dorso
lateral prefrontal system impairs OR performance
review see Oscar-Berman, 1991)
Bodis-Wollner et al.
found PD patients to be impaired on a DR
task, but Freedman and Oscar-Berman (1986b) found
only demented PD patients to be impaired on OR.
Specifically, in a comparison of DR and DA perform
ance among non-demented PD, demented PD and
Alzheimer's disease (AD) groups, Freedman and
Oscar-Berman (1986b) found demented PD to be
impaired on DR only, whereas the AD group was
impaired on DR and DA.
That DR might be impaired in only more severely
affected PD patients is supported by findings re
ported by Owen et al. (1993), using a spatial recogni
tion task akin to DR. In this task, subjects are shown
during the presentation phase a series of five unfilled
white spaces, one at a time, in different locations on
a computer screen. In the recognition phase, two
spaces appear simultaneously and subjects have to
select which of the two locations was used in the
presentation phase. Auditory and visual feedback
on the (in)correctness of responses is provided after
each response. On this task, only PD patients who
were medicated and who had severe symptoms were
impaired. In sum, the preponderance of findings
suggests that delayed response might be sensitive
to only more severely affected PD patients' patho
Source memory. Another measure thought sensi
tive to frontal dysfunction (and to depend on tempo
ral memory) is source memory
(Janowsky et al.,
. Source memory refers to the ability to recall
"where and when" information was learned, rather
than content. Taylor et al. (1990) attempted to study
source memory in early PD using a modification of
the California Verbal Learning Test
(CVLT; Delis et
. Unfortunately, their results were ambigu
ous, because PD patients were impaired relative to
normal controls in identifying the source of words on
one list but not another. However, Taylor et al.'s
(1990) findings, in combination with those of another
(Goldman et al., 1994)
, indicate the
possibility that source memory might be differentially
affected in PD and the earliest stages of AD. Whereas
Taylor et al. (1990)
found suggestive evidence of
impaired source memory in PD,
Goldman et al.
found that early AD patients, once matched
to normal controls for made-up fact recall, performed
similarly to the control group on a test of source
memory. Together, these findings suggest the poten
tial dissociability of fact and source recall in PD and
AD, a finding also reported in amnesics and frontal
(Janowsky et al., 1989b; Shimamura
and Squire, 1987, 1991)
Subject-ordered tasks. The demand common to
subject-ordered tasks is the requirement that subjects
organize and execute a sequence of responses without
the external imposition of a sequence by the experi
menter. Such tasks have been shown to be sensitive
to frontal dysfunction
(e.g. Petrides and Milner, 1982)
and medicated PD patients have been shown to be
impaired on a subject-ordered pointing task (Gotham
et al., 1988). A task akin to subject-ordered tasks is
the spatial working memory task employed by Owen
(1990, 1992, 1995a)
. In this task, subjects are
required to search through boxes presented on a
computer screen so as to collect tokens contained in
the boxes. At any given time, only one token is
hidden in a box, and the subject is instructed to
search until that token is found. Once used to hide a
token, that box is not used again to hide another
token, and subjects are instructed to this effect.
On this task, which has been shown to be particu
larly sensitive to frontal lobe lesions
(Owen et al.,
, both mildly and severely affected, medi
cated PD patients demonstrate impairments
et al., 1992, 1993)
. However, the impairment of PD
patients and individuals with frontal lesions is qualita
tively different. Specifically, the task allows computa
tion of at least two scores: errors (i.e. boxes revisited
in which a token was already previously discovered)
and strategy. An efficient strategy involves following
a predetermined search sequence, and always starting
a new search from the same box.
Owen et al. (1992)
thus quantified strategy by determining the number
of searches started from the same and different boxes.
Whereas frontal lesion patients performed poorly
both in terms of the number of errors and strategy
(Owen et al., 1995b)
, medicated PD patients
made more errors than the normal control subjects,
but their strategy use was comparable to that of
control subjects (Owen et al., 1992). These findings
together again suggest that memory deficits of PD
patients may be at least qualitatively different from
those observed in frontallesion groups.
Conditional associative learning. In conditional
associative learning tasks, a subject is typically first
taught to make a series of responses (e.g. hand ges
tures). The next step involves the subject learning to
which one of several external signals each gesture is
appropriate. For example, each of several distinct
visual stimuli (e.g. different colored lights) signals
that a particular gesture is appropriate. Numerous
learning trials are administered, so that if a subject
makes an inappropriate response, the subject per
forms the other possible responses until the correct
response is produced to that given stimulus. The
usual measure of interest is trials-to-criterion (a pre
determined number ofconsecutive, correct responses).
Patients with frontal lesions have been shown to
have difficulty learning these associations
. PD patients have been noted to also be
impaired on conditional assocIatIve learning
(Gotham et al., 1988; Sahakian et al., 1988; Taylor et
. However, this effect was only reliably
observed in medicated PD patients in the Gotham et
al. (1988) and
Sahakian et al. (1988)
Canavan et al. (1989a) found early PD patients to
perform normally on two conditional associative
learning tasks. In addition, memory for hand gesture
sequences is apparently impaired in individuals with
frontal lesions but not PD
(Canavan et al., 1989b)
Summary of issues arising from studies of PD
patients' performance on "frontal" memory
tests. Experimental studies of PD patients' perform
ance on "frontal" memory tests perhaps provide the
most convincing evidence to date that frontostriatal
dysfunction underlies select memory impairments in
PD. A major conceptual issue remains, however.
Namely, does a frontally related core defect in tempo
ral memory underlie PD patients' impaired perform
ance on all memory tasks? Results of two studies
suggest that this might not be the case. A recent study
by Parkin and Hunkin (1993) has indicated that
frontal pathology may be a necessary condition for
impairments in temporal dating of events in remote
memory, but that it may not be a necessary condition
for impairments in anterograde temporal context
memory. This raises the possibility that deficient
anterograde and remote temporal memory in PD
are mediated by different cognitive and neural
The possibility that different mechanisms underlie
impaired temporal ordering and conditional associa
tive learning in PD was suggested in a recent study
Vriezen and Moscovitch (1990)
. On the temporal
ordering task, subjects were required to reproduce
from memory a series of stimuli in the order of
Vriezen and Moscovitch (1990)
puted indices of the extent to which subjects pre
served the absolute and relative order of stimuli.
Absolute position was defined as the sum of the
distances between the presentation and recall posi
tions of the stimuli. Relative deviation was calculated
by summing the distance between "each stimulus'
presentation position and the presentation position
of the stimuli placed before and after it on recall".
With respect to the temporal ordering task, PD and
control subjects did not differ in terms of the number
of stimuli placed in the correct position [contrary to
Breen's (1993) findings], but PD patients performed
more poorly than controls in preserving the relative
order of stimuli.
Vriezen and Moscovitch (1990)
proposed that whereas maintenance of the absolute posi
tion of stimuli involves relatively automatic processes,
recall of the relative position involved more strategic,
self-initiated processes. They thus suggest that com
promised strategic retrieval processes underlie certain
aspects of deficient temporal memory (i.e. relative
order). A similar explanation is offered for the finding
that PD patients were impaired on conditional asso
ciation learning when a trial-and-error learning para
digm was used, but not when an immediate feedback
paradigm was employed. The authors caution, how
ever, that it is premature to accept that a common
mechanism underlies PD patients' impairments on
trial-and-error conditional associative learning and
recall of relative temporal order, because perform
ances on these two tasks were not strongly correlated.
Vriezen and Moscovitch (1990)
point out that differ
ent regions of the frontal lobes may be critical to the
performance of the two tasks, or that the two tasks
demand only overlapping (i.e. both shared and
unique) cognitive processes.
Functional imaging and memory test performance in PD
Goldenberg et at. (1989
) found non-demented PD
patients' impairments in set shifting and attentional
control to be related to frontal and parietal blood
flow abnormalities on SPECT, but it is unclear if
similar pathophysiology and cognitive deficits
account for memory impairment. Only two studies
have attempted to directly establish a link between
brain physiology and memory test performance in
Demonet et al. (1994)
examined regional cerebral
blood flow (rCBF) activation during passive listening
and memorization of a word list in 18 early PD
patients and 20 normal control subjects. These au
thors found that different regions were activated in
the two subject groups during the listening and mem
orization tasks. In the control group, memorization
was accompanied by increased rCBF in five left-sided
regions: anterior middle frontal, posterior inferior
frontal, superior middle temporal, thalamic and len
ticular. In the PD group, memorization of the word
list was associated with activation of only the superior
prefrontal regions. Because the PD subjects' recall
was comparable to that of the control group, De
monet et at. (1994) interpreted their findings as sug
gesting the operation in PD of a compensatory
memory mechanism supported by the superior pre
frontal regions. This raises the possibility that once
such a frontally mediated compensatory mechanism
fails, PD subjects develop memory dysfunction,
although it is also possible (because correlations
between rCBF changes and recall scores were not
reported) that the frontal activation observed reflects
activation of on-line processes important to adequate
recall. Similarly, although
Holthoff et al. (1994)
found impaired verbal memory to be related to PET
imaged [IBF]-dopa uptake reductions in the striatum,
the role of possible executive deficits or on-line pro
cesses in memory was not investigated.
SOME REMAINING ISSUES ABOUT THE
FRONTAL COGNITIVE DYSFUNCTION
HYPOTHESIS OF PD MEMORY IMPAIRMENT
The proposal that PD memory deficits are related to
cognitive changes associated with frontal dysfunction
is attractive from anatomical and pathological stand
points. First, the striatum and frontal cortex are
intimately connected via a series of parallel circuits
(Alexander et al., 1986; Cummings, 1993; Mega and
and some of these subcortical cir
cuits are in tum connected to regions important to
memory, such as entorhinal cortex
Zola-Morgan and Squire, 1993)
. Consequently, it is
plausible that PD striatal pathophysiology has an
effect "downstream" on the frontal cortex and on
entorhinal cortex and hippocampus. Second, PD
might involve pathology of the frontal cortex itself.
For example, a reduction of GABAergic receptor
density in the frontal cortex of PD patients was
reported by Griffiths and Crossman (1992), and re
duced frontal cerebral blood flow and oxygen metabo
lism were observed in PD by Wolfsen et al. (1985).
Furthermore, Demonet et al.'s (1994) study indicates
that frontal cerebral blood flow may be related to
PD patients' performance on a memory task. As
plausible as the "frontal cognitive dysfunction" expla
nation of PD memory deficits may appear from an
anatomical standpoint, the empirical neuropsycho
logical evidence attempting to demonstrate the "fron
tal" nature of PD memory deficits is tenuous.
Perhaps the strongest evidence to date that frontal
dysfunction in PD can impair memory comes from
studies employing experimental memory tasks specifi
cally sensitive to frontal lesions. This by no means,
however, implies that impairments shown by PD
patients on standardized memory tests are also attrib
utable to frontal dysfunction. Several factors make it
difficult to accept as convincing that all PD memory
deficits are exclusively a by-product of executive defi
cits related to frontal dysfunction. First, there are
few direct comparisons of neuropsychological deficits
in PD and frontal lesion groups which might provide
evidence about the extent to which cognitive deficits
in PD resemble those associated with frontal dysfunc
tion. However, even if comparisons among PD and
frontal lobe lesion patients' performances on tests of
executive functions and memory were forthcoming,
they involve several methodological and conceptual
difficulties. Methodological concerns regard the com
parability of frontal lesion and PD groups on vari
ables which might impact cognition. For example,
whereas frontal lesions might be the result of acute
and relatively static events (such as cerebrovascular
accidents or surgery), PD is a chronic, progressive
disease. Comparability of frontal lesion and PD
groups might also be affected by medical regimens of
PD patients which can impact frontal cognitive func
tions and memory in a differential manner
et al., 1993)
. Yet another variable on which frontal
lesion and PD patients will have to be equated before
valid comparisons can be made of the quality of their
memory problems, is overall severity of cognitive
(see Sagar, 1991)
; .otherwise quantity and
quality of impairments are confounded.
One difficulty in relating memory deficits to frontal
dysfunction in PD is the fact that the role of the
frontal lobes in memory remains debated
Benson, 1984; Schacter, 1987; Shimamura et al.,
. Even when frontal dysfunction is associated
with circumscribed memory deficits, the neuropathol
ogy and cognitive deficits observed in frontal patient
groups are extremely heterogeneous
(Stuss et al.,
, thus making it difficult to establish and describe
the mechanisms underlying memory deficits. Given the
variability of frontal and PD patients' performances
on memory tasks
(Beatty, 1992b; Stuss et al., 1994)
and given the fact that anyone or more of several
converging fronto-subcortical circuits might be
compromised in PD
, one issue con
fronting researchers is whether one or several cogni
tive mechanisms underlie PD memory impairment.
Certainly, the work of
Vriezen and Moscovitch (1990)
suggests that different cognitive mechanisms may
underlie impaired performance on memory tasks
seemingly tapping a similar cognitive mechanism. To
this end, it becomes important to identify a measure
of memory sensitive to pathology in a large range of
frontal regions. Correlation of such a measure with
other memory and executive function measures might
clarify if a common mechanism underlies memory
impairment in PD. Work by
Stuss et al. (1994)
significance in this regard. Specifically,
Stuss et al.
found an impairment in subjective clustering
of word lists
(Sternberg and Tulving, 1977)
to be the
common thread in the performances of patients with
left, right or bilateral lesions in the dorsolateral,
medial, septal and striatal frontal regions. That is,
frontal lesion patients did not "pair" the same words
consistently across recall trials, such that a word
following another during recall on one trial tended
not to follow that same word again on subsequent
recall trials. Whether PD patients demonstrate dimin
ished subjective clustering awaits empirical
In the absence of "frontal" comparison groups,
one of the principal investigative strategies has fo
cused on correlating (or covarying) PD patients' per
formances on memory tests and tests purportedly
sensitive to frontal lobe dysfunction, especially the
Wisconsin Card Sorting Test
(WCST; e.g. Bondi et
al., 1993; Pillon et al., 1993)
. Several methodological
and conceptual problems attend such an approach
. One difficulty is that impaired
WCST performance is not specific to frontal lobe
(Heaton, 1981; Anderson et al., 1991)
and, given the complexity of the test, likely multideter
mined. Indeed, some suggest that no clinical neuro
psychological test has been shown to be specifically
sensitive to frontal dysfunction
(Reitan and Wolfson,
. Other obstacles to correlational studies include
the observations that the error patterns of PD and
frontal patients on the WCST may diverge (Beattyet
al., 1989a), and that WCST performance is highly
variable across PD samples
Even if one were to temporarily suspend these
methodological and conceptual objections, the data
from correlational studies to date still do not strongly
support a frontal cognitive dysfunction explanation
of memory impairment in PD. It bears emphasizing
that the statistical significance attached to a correla
tion coefficient merely conveys the probability that
the observed relationship between two variables is
due to chance or error. With a sufficiently large
sample size, even very small correlation coefficients
become statistically significant. As
Allen and Yen
have pointed out, the most common interpreta
tion of a correlation coefficient is made in terms of
its square, which conveys the proportion of the vari
ance in one variable accounted for by its linear rela
tionship with another variable. A survey of the
correlation coefficients reported indicates that the
variance in memory test scores attributable to frontal
cognitive test scores ranges from 4% to 50%, with
the preponderance of values falling into the lower
end of this range. Furthermore, these values are
likely overestimates given the intercorrelation among
variables. This strongly suggests that frontal cognitive
functions can impact performance on memory tasks,
but that they are unlikely to be the sole or even
principal determinants of memory test performance.
The assertion that frontal cognitive dysfunction
underlies memory deficits in PD is also confronted
by the challenge that frontal cognitive functions and
memory may be differentially affected by pharmaco
logical manipulations of the dopaminergic system.
Lange et al. (1992
, 1993) reported comparisons
among PD patients' performances on several frontal
cognitive function and memory tasks, both on and
off levodopa. Whereas performance on three "fron
tal" tasks (Tower of London, spatial working
memory and attentional set-shifting) was superior on
than off levodopa, performance on three tasks with
significant declarative memory and lesser working
memory demands (pattern and spatial recognition,
delayed matching to sample and visuospatial associa
tive learning) was comparable on and off levodopa.
Not only do these findings suggest that different
neurochemical substrates mediate frontal cognitive
functions and memory, but they provide a clear disso
ciation among these functions, thus suggesting that
performance on at least some memory tests can be
relatively independent of frontal cognitive functions.
Furthermore, not all frontal cognitive functions may
be similarly affected by levodopa. For example,
Gotham et al. (1988)
found that performances on
conditional associative learning and subject-ordered
pointing were impaired on levodopa, whereas verbal
fluency was impaired off levodopa, and WCST per
formance was impaired both on and off levodopa.
Owen et al. (1995b) found that even different meas
ures derived from the same task could be differen
tially affected by levodopa treatment. Specifically,
levodopa-treated PD patients, relative to an unmedi
cated group, showed better planning accuracy on the
Tower of London, but similar (perhaps somewhat
larger) latencies. The diversity of empirical findings
concerning PD memory impairment suggests that it
is important to develop a theoretical framework
which accommodates these findings.
TOWARD A DISTINCTION BETWEEN
PROSPECTIVE AND DECLARATIVE MEMORY
IMPAIRMENT IN PD?
The distinction between declarative and non-declara
(see Squire, 1992)
is well accepted, and
it has received empirical validation from studies of
PD. Another concept, namely prospective memory
(Meacham and Leiman, 1982)
, has only recently
begun to receive attention in neuropsychology
Dalla Barba, 1993)
Meacham and Leiman (1982)
drew a distinction between retrospective and prospec
tive remembering. Whereas retrospective memory
refers to the recollection of information from the
past (and most clearly resembles what has been re
ferred to as declarative memory), prospective remem
bering concerns itself with recalling actions to be
FIG. 1. Simplified representation of the possible interactions
among executive, declarative and prospective memory
performed in the future. As
Hitch and Ferguson
pointed out, prospective memory can thus be
conceptualized as involving the following stages:
forming an intention; remembering the intention
during an intervening period; and performing the
intended action at the appropriate time.
study provides a useful exemplar
to distinguish prospective and retrospective memory.
Retrospective memory might be exemplified by recall
ing the names of films one has seen in the past.
Prospective memory, in contrast, might be exempli
fied by recalling which films one intends to see in the
future and when. One measure of prospective
memory, then, might be the person's actual attend
ance at films intended to be seen. A priori one might
expect frontal cognitive functions to play a central
role in prospective memory. Prospective memory has
a strong temporal component, and we have already
reviewed research demonstrating the sensitivity of
temporal memory to frontal dysfunction. In addition,
prospective memory requires coupling of an action
with an intended goal. The role of the frontal lobes
in controlling actions by their intended results has
been consistently demonstrated
Dalla Barba (1993) has pointed out that prospective
memory also requires access to declarative memory
or retrospective remembering. A simplified schematic
of the potential relationships among executive func
tions, declarative memory and prospective memory is
presented in Fig. 1.
In general, studies with normal subject populations
have shown that performances on prospective and
retrospective memory tasks are not significantly corre
(Kvavilashvi1i, 1987; Einstein and McDaniel,
1990; Maylor, 1990; but see Hitch and Ferguson,
. The only study investigating prospective
memory in dementia
(Huppert and Beardsall, 1993)
suggests that a similar lack of correlation between
prospective and retrospective memory might also be
obtained in neurologic populations. It is, however,
premature to elevate prospective and declarative
memory to the stature of independent memory sys
tems. For one, prior studies generally leave un
addressed the extent to which executive functions,
prospective memory and declarative memory are dis
sociable. In addition, the definitions of executive
functions, prospective memory and declarative
memory blur. For example, some content of prospec
tive memory, including intentions, can be "declared",
and it is unclear if difficulty in some executive func
tions (e.g. monitoring) can differentially impact pro
spective and declarative memory, or impact memory
but not other domains of cognition. Finally, as
and Ferguson (1991)
have pointed out, the apparent
lack of correlation between prospective and retrospec
tive memory does not exclude the possibility that
similar principles apply in prospective and retrospec
tive memory. Until such issues are more adequately
addressed empirically, a simpler distinction may be
Shimamura et al. (1991)
proposed that the definition
of prospective memory might beneficially be expanded
to cover "processes and strategies involved in plan
ning, monitoring, and organizing memory, not just
actions" (p. 191). If such a definition of prospective
memory is accepted, Shimamura et al.'s (1991) review
of studies of frontal and amnesic patients makes it
clear that prospective and declarative memory can be
dissociated in neurologic populations, and that an
impairment in one does not necessarily imply an
impairment in the other. More specifically, Shima
mura et al. (1991) review empirical evidence indicating
that individuals with frontal lobe lesions have impaired
prospective memory, despite performing normally on
what have traditionally been described as declarative
memory tasks (i.e. tests of new learning). In contrast,
amnesic patients perform well on numerous prospec
tive memory tasks, but fail declarative memory tasks.
Several studies suggest that dissociations between
prospective and declarative memory impairments,
analogous to those described by
Shimamura et al.
among frontal lesion and amnesic patients,
might be obtained within PD. Mohr et al. (1990), for
example, have described impaired declarative
memory in the face of preserved prospective memory,
whereas the converse pattern of performance was
Owen et al. (1992)
, at least in the mild
PD groups. Indeed, the findings of
Cooper et al. (1993)
, and data highlight
ing the dissociability of the effects of pharmacologic
manipulation on memory and executive functions
(Lange et al., 1993) can also be interpreted as demon
strating a dissociation between prospective and de
clarative memory impairments. In addition to the
two possible subgroups of PD patients showing con
verse patterns of impairment and preservation of
declarative and prospective memory, a likely sizeable
third PO subgroup demonstrating impairments in
both prospective and declarative memory exists. This
can be inferred from the studies demonstrating a
relationship (albeit typically a modest one) between
performance on frontal cognitive tasks and declara
tive memory tests. Together, findings of the studies
reviewed here point to the possibility that declarative
and prospective memory are separable, yet linked.
One possible agenda faced by PD memory research
guided by a declarative/prospective memory distinc
tion is the delineation of how executive functions,
prospective memory and declarative memory are re
lated. More specifically, research might address which
executive functions relate to prospective memory im
pairment, and whether the same executive functions
significantly impact declarative memory. The identifi
cation and comparison of processes underlying pro
spective and declarative memory might be of mutual
benefit to neuropsychology and cognitive psychology.
Such studies might further the understanding of cogni
tive mechanisms underlying PO memory impairment,
and simultaneously subject to empirical scrutiny the
prospective vs declarative memory distinction. If the
prospective/ declarative memory distinction is empiri
cally supported, the behavioral neurology of PO
might be informed by evaluating whether the three
PO subgroups defined here on the basis of memory
impairments bear any relationship to the three PO
subgroups defined by Cummings (1988b) on the basis
of different neurotransmitter abnormalities.
We conclude that the prospective/declarative di
chotomy provides one framework within which to
organize the diverse empirical findings concerning
PD memory impairment reviewed here. The frame
work also permits formulation of a research agenda
within which frontal cognitive functions are seen less
as an obstacle to understanding PD memory impair
ment but rather, as
has advocated, a
means of obtaining insights into the nature of normal
memory not easily gleaned from the study of pure
Preparation of this manuscript was supported in part by
NIA Grant AG 10182. The authors thank Dr William W.
Beatty and two anonymous reviewers for their insightful
and helpful comments on an earlier version of this
A.I. TROSTER AND I.A. FIELDS
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(Received 8 February 1995; accepted as revised
13 July 1995)
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