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Michigan State
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This is to certify that the

thesis entitled

DEPTH 0F PROCESSING AS AN INDEX OF FRONTAL
LOBE AND MEMORY FUNCTIONING IN OLDER ADULTS

presented by
David Dean Cordry

has been accepted towards fulfillment
of the requirements for i
i

M.A. Psychoiogy

degree in

[L M

Major professor

 

 

 

[hue August 28, 1998

 

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DEPTH OF PROCESSING AS AN INDEX OF FRONTAL LOBE AND MEMORY
FUNCTIONING IN OLDER ADULTS
BY

David Dean Cordry

A THESIS
Submitted to
Michigan State University
in partial fulfillment of the requirements
For the degree of
MASTER OF ARTS
Department of Psychology

1998

ABSTRACT

DEPTH OF PROCESSING AS AN INDEX OF FRONTAL LOBE AND MEMORY
FUNCTIONING IN OLDER ADULTS

BY
David Dean Cordry
An analysis of the relationship between the type of
strategies used on a verbal fluency test and a verbal
learning test in older adults was conducted. A significant
positive relationship was between use of complex strategies
on a verbal fluency task and use of complex strategies
during retrieval on a verbal memory test. Use of semantic
clustering strategies on a verbal fluency test was a
significant predictor of use of semantic strategies on a
verbal memory test. The results are discussed within the
context of a deficiency in depth of processing as one
component of age related memory loss, and the involvement

of the frontal lobes in these processes are discussed.

ACKNOWLEDGEMENTS

I would like to express my gratitude to my mentor and
chairperson, Dr. Abeles for all of his guidance and support
in the writing of this thesis. Furthermore, I would like to
thank my other committee members, Dr. Hurley, and Dr. Nigg
for their insightful comments and criticisms that helped
guide this work.

I would especially like to thank my friends and
colleagues in the department, as well as my family for their
support and encouragement.

Finally, and most importantly, I would like to thank my
wife, Meg for all of her love, help, and support. Without
her this step in my pursuit of erudition would not have been

possible.

iii

TABLE OF CONTENTS

INTRODUCTION .......................................................................... l
Attentional Processes ............................................. 2
Memory Functioning ................................................... 6
Research Data for Older Adults ............................... 8
Age Consistent Memory Decline ............................... 9
Frontal Lobes ............................................................ 12
Verbal Fluency: Semantic and Phonemic
Associations ................................................................ 15
Aims of Current Study .............................................. 19
Hypothesis 1 .............................................................. 22
Hypothesis 1a ............................................................ 22
Hypothesis 2 .............................................................. 22
Hypothesis 3 .............................................................. 22

METHODS ................................................................................. 22
Participants ............................................................... 22
Measures ...................................................................... 23

RESULTS ................................................................................. 27
Hypothesis 1 ............................................................... 28
Hypothesis 1a ............................................................. 28
Hypothesis 2 ............................................................... 29
Hypothesis 3 ............................................................... 29

DISCUSSION ............................................................................ 30

REFERENCES ........................................................................... 4O

IN TRODUCT I ON

As the population of older adults continues to grow, so
does the importance of understanding the processes that
accompanies aging. Serious cognitive problems have been
diagnosed in 15~25% of adults over the age of 6S and the
number rises to 70% in nursing homes and other institutional
settings (Knight, Teri, Wohlford, & Santos, 1995). Some
degree of cognitive decline and memory loss are typically
assumed to be a part of the aging process. However, organic
mental disorders are overdiagnosed in the elderly (La Rue,
1992). Understanding the process and extent of cognitive
decline and memory loss in older adults is essential to
being able to make the distinction between normal aging and
organic disorders.

Some evidence of intellectual function decline has been
demonstrated by research, although significant decline does
not reliably occur until the 70 or 80 year age range (Birren
& Schaie, 1977; Benton, Eslinger & Damasio, 1981).
Furthermore, the documentation of cognitive deterioration in
the elderly is largely dependent on the neuropsychological
tests employed. Certain intellectual functions tend to
remain more intact, such as verbal skills, while nonverbal,
visuospatial skills tend to decline more sharply in older
adults (Hochanadel & Kaplan, 1984). The pattern of decline
of nonverbal abilities in old age has been referred to as
the "classical aging pattern" by Hochanadel and Kaplan

(1984). Horn and Cattell (1967) described this distinction

as "crystallized" intelligence which subsumes factual and

cultural assimilation that occurs throughout the life-span,
versus "fluid" intelligence which includes problem-solving
abilities and capacity to deal with novel tasks that tends

to decline with aging.

Attentional Processes

 

When questioned regarding the most troubling aspects of
cognitive decline, the elderly often mention memory
difficulties and lapses in attention and concentration.
Despite the absence of a widely accepted definition of the
term attention among scientists, some older adults are aware
of the kinds of their attention problems and the effect that
lapses in attention have on their ability to remember. The
phrase "paying attention" suggests both that attention can
be consciously focused and that its intensity level has
certain costs to attention resources (van Zomeren & Brouwer,
1994). Age-related changes of attention processes are of
primary importance in understanding cognitive decline in the
elderly; Stankov (1988) suggests that changes in fluid
intelligence in older adults are dependent on changes in
attentional processes.

Elucidating the impact that attention has on other
areas of cognitive functioning in the elderly requires
breaking down attention into its specific functions.

Components of attention include concentration, perceptual

speed, attentional flexibility, selective attention, and
freedom from distraction (van Zommeren & Brouwer, 1994).

Concentration, or sustained attention is the ability to
maintain mental effort on tasks. Given the length of some
neuropsychological batteries, decrements in sustained
attention resources of older adults are presumed to occur.
-However, the research seems inconclusive regarding the
existence of an age decrement in sustained attention.
Surwillo and Quilter (1964) found that older and younger
adults were about equally capable in detecting a target over
the first 15 minutes of a 62 minute task, but that the older
registered a greater decrement in sustained attention during
this task's last 15 minutes. Stankov (1988) found that a
concentration factor was significantly negatively correlated
with age. However, in contrast to these findings, Giambra
and Quilter (1988) found that while the likelihood of
detecting the target decreased over time, this occurred at
an equal rate in older and younger adults.

Another facet of attention is perceptual speed or
searching defined as the ability to find a specific target
within an array of similar targets. Research by Plude and
Doussard—Roosevelt (1989) examined the approach to visual
search tasks in younger and older adults and found that
although they used similar approach strategies, older adults
required twice as long to consider each item. These results
seem consistent with a theory of generalized reduction in

energy for cognitive processing, resulting in a

slowing effect (Salthouse, 1988).

Attentional flexibility, described as the ability to
shift attentional resources from one task to another, is
another aspect of attention that may decline in older
adults. Stankov's (1988) factor analysis identified an
attentional flexibility factor that correlated negatively
and significantly with age. Furthermore, when the effects
of the attentional flexibility component were partialled
out, age-related decline in fluid intelligence was
essentially eliminated. Age-related difficulties in
shifting attention are similar to the reduced capacity to
shift attention that Luria (1973) found in patients with
frontal lobe pathology. Indeed, a study by Teece (1978)
implicated the involvement of the frontal system, as
measured by evoked potentials, in the ability of older
persons to change attention to a different task.

The ability to attend to a particular stimuli while
ignoring other, distracting stimuli is described as
selective attention. Layton (1974) found a decrement in
this aspect of attention for simple stimuli. In this study,
participant's were required to detect a target out of a
large array; elderly participant's were more penalized by
this distracting information. Deficits in selective
attention have been consistently demonstrated in older
adults (see Hochanadel and Kaplan, 1984 for review). Hasher
and Zacks (1988) hypothesized that inhibitory functioning is

reduced in older adults, as evidenced by more frequent

intrusions of personal memories into recall of text. A
reduced ability to filter out irrelevant information would
seem to explain the difficulties some elderly participants
have on tasks that require selective attention. One
hypothesized mechanism for this decrement in inhibitory
functioning has been suggested by Arbuckle and Gold (1993)
as a frontal lobe deficit. The involvement of the frontal
system in specific inhibitory deficits has received other
support. Kramer, Humphrey, Larish, Logan, and Strayer
(1994) found that older adults exhibit deficits in
inhibitory processing on a task in which processing has been
linked to frontal lobe function.

Tasks that require subjects to divide their attention
for successful performance show substantial age effects
(McGhie, Chapman, & Lawson, 1965; Craik , 1973). Divided
attention is another aspect of attention functioning that
has demonstrated a consistent decrement in older adults
relative to younger adults; that is, older adults are more
penalized on tasks that require the allocation of their
attentional resources between two tasks simultaneously (see
Hartley, 1992 for review).

The abilities to divide attention, suppress irrelevant
stimuli, and shift attention to new tasks are critical to
performance on neuropsychological tests. In particular, the
relationship between attention deficits and memory problems
has been demonstrated (Craik & Lockhart, 1972). If a

stimulus to be remembered does not receive focused attention

of sufficient intensity it will not be entered into memory.
Furthermore, the concept of working memory--the conscious
rehearsal of information in an attempt to remember it in the
long term--is as much a concept of attention as it is of
memory (Baddeley, as cited in van Zomeren & Brouwer, 1994).
Working memory requires focused attention in the rehearsal
of information; therefore, the impact on memory, of a
reduced ability to inhibit distracting information during
this rehearsal can be clearly seen. In order for memory to
occur, attention must precede it. Understanding the extent
to which attentional processes are compromised, as well as
the mechanisms responsible for this loss, are of particular
importance in examining the specific memory function

declines that older adults experience.

Memory Functioning

 

One of the most consistent complaints of the elderly is
of memory decline (Lowenthal, Berkman, Buehler, et a1.
1967). One of the primary concerns of older adults is the
loss of memory ability. In a study by Lowenthal, Berkman,
Buchler, Pierce, Robinson and Trier (1967) over 50% of
elderly respondents reported a decline in their memory
function. However, demonstration of actual memory decline
in elderly populations has been largely dependent on the
specific aspect of memory being measured. Information-

processing models have been used to understand the process

through which to-be-learned material is entered into memory
and recalled.

The initial stage of memory has been conceptualized as
sensory memory (La Rue, 1992). In this stage of memory,
external stimuli is assumed to be provided with a fairly
complete representation, although this image is subject to
rapid decay if deeper processing is not engaged in. An
example of this stage of memory includes, registering the
specific letters of a presented stimuli (e.g. having a
representation of the letters that compose the name of a
newly introduced person). The deficits of older adults in
sensory memory function has been demonstrated by research
(Cerella, Poon & Fozard, 1982; Walsh, Till, & Williams,
1978). These investigators found that older adults require
increased exposure to material in order for an adequate
image to be generated. Furthermore, when longer
presentation of stimuli is allowed for, age is not a factor
in the rate of decline (Botwinick, 1973).

Primary or short-term memory is conceptualized as a
temporary memory store that requires rehearsal of to-be-
remembered items and focused conscious attention. The
capacity of this primary memory is limited to the number of
items that can be consciously rehearsed. Despite subjective
reports of the elderly that they are experiencing short-term
memory decline, objective research measures have not
consistently demonstrated the presence of short-term or

primary memory impairment, at least through age 70 (Craik,

1977). Secondary memory is conceived of as a cache of
essentially permanent acquired knowledge. Learning of new
information occurs when the new material has been encoded
into secondary memory, a process which may be one source of

memory difficulty in the elderly.

Research Data for Older Adults

 

Thirty older adults were equivalent to young adults in
their ability to recognize probe words from a short list of
items after presentation (Lorsbach & Simpson, 1984). In
this experiment subjects were required to determine if a
probe word was identical, sounded the same, or meant the
same thing as, one of the ten words in a list of to-be-
remembered items. Although older adults were equivalent to
younger adults in the identical trial, they were slower than
younger adults in recognizing synonyms of list items; thus,
the implication from this study being that while the elderly
exhibit no deficits relative to younger adults in the
functioning of primary memory, the encoding of more
elaborate information, such as meaning may be more difficult
for the elderly. Older adults typically engage in less
efficient encoding strategies during initial presentation of
the new material; Sanders, Murphy, Schmitt and Walsh (1980)
found that the elderly use less efficient learning
strategies-—repetition as opposed to organizatonal
strategies--and engage in such strategies less actively.

Furthermore, Hulicka and Grossman (1967) found that most

older adults did not report spontaneously employing mnemonic
techniques when learning a list of verbal paired associates,
while most young adults admitted to using some type of

association strategy.

Age Consistent Memory Decline

 

The utilization of semantic information during encoding
represents a complex operation that requires more time than
more superficial encoding based on the pronunciation or
perceptual characteristics (Posner, 1978). Indeed, there is
some evidence that older adults have more difficulty in
using semantic information to enhance the processing of
material to be remembered.

One explanation for this deficit in efficiency of
encoding in older adults has been proposed by Salthouse
(1982) as a generalized slowing of processing speed that
accompanies aging. According to Salthouse, the elderly
require more time to engage in more efficient encoding, and
are consequently penalized more than younger adults in most
experimental paradigms. Furthermore, if the processes
involved in the organization of material to be learned, or
deeper encoding, are assumed to require more time than
superficial encoding, then a speed-loss explanation seems to
account for the difficulty that older adults demonstrate in
utilizing more elaborate, semantic processing. Simon (1979)
found some support for this hypothesis by demonstrating that

while semantic cues decreased in effectiveness for retrieval

in the elderly, younger adults demonstrated a similar
pattern when the presentation rate of to-be-learned items
was increased. However, Lorbasch and Simpson (1984) found
that the manipulation of presentation

rate did not selectively impair older adults when the
processing of meaning was required, suggesting that the
speed-loss hypothesis can not fully account for the
difficulty older adults exhibit in encoding semantic cues of
to-be-learned material.

An additional explanation for this age-related memory
decline has been proposed by Craik (1977) as a deficiency in
the depth of processing used by older adults. One
representation of this is the utilization of phonemic and
semantic characteristics of words. Phonemic cues are
associations between words based on the pronunciation
characteristics. In a list of words to be remembered, the
clustering of words with similar sounds (e.g., farm, fake)
would represent a phonemic strategy and a more surface-level
of processing. On the other hand, semantic cues are
associations based on related meanings of words, require
more elaborate processing, and produce stronger memory
connections (Craik, 1977). This type of strategy would be
demonstrated by the clustering of words from a list of to be
remembered items that belong to the same meaning category
(e.g., apricot, apple). Hulicka and Grossman (1967) found
that older adults were less likely to incorporate a semantic

encoding strategy on a verbal learning task than

10

were younger adults. However, when elderly participants are
instructed to use more elaborate types of organization on a
memory task, they improve more than do younger participants,
although they still perform at a lower overall level than
younger adults (Hulicka, Sterns & Grossman, 1967).
Furthermore, phonemic cues--which represent a less elaborate
level of processing-—were more effective for older adults in
a recall task than were semantic cues, suggesting that older
adults suffer from a reduced ability to process information
at deeper levels (Simon, 1979).

These results suggest that older adults tend to utilize
features of to-be-learned material that are perceptually
prominent, rather than using the meaning of to-be—learned
material. In other words, this means that older adults tend
to rely on a phonemic strategy as opposed to a more
elaborate and effective semantic one (Craik, 1977).

This pattern of being bound to perceptual features of
stimuli is characteristically seen in the performance of
patients with frontal lobe pathology on memory tasks
(Goodglass & Kaplan, 1979). Thus, deterioration of the
frontal lobes has been hypothesized as a contributing
mechanism to the cognitive and memory decline specific to
older adults. The frontal system is implicated in the
allocation of attention, planning and beginning of complex
activity, the ability to screen out irrelevant information,
and monitoring and adjusting behavior in response to

feedback (Luria, 1973).

ll

Frontal Lobes

 

Evidence for decreased functioning of the frontal lobes
in older adults has been found in research with
neuropsychological measures. A study by Mittenberg,
Seidenberg, O'Leary, and DiGiulio (1989) compared the
performance of older and younger adults on several
neuropsychological measures of lateralized and focal
function. Frontal-lobe measures accounted for more variance
in relation to age than did measures of parietal or temporal
functioning (1989). Anatomical studies by Haug (as cited in
Mittenberg et al., 1989) found that neuronal loss was
pronounced in the frontal lobes of the elderly. Further
evidence for the possibility of a decrement of frontal lobe
functioning in the elderly was found by Veroff (1980). A
qualitative analysis of the visual reproductions of older
adults revealed that the segmentation of strategy and
perseverations seen in patients with frontal system
pathology was also demonstrated by elderly participants
(1980).

Certain problem-solving tasks, which require frontal-
lobe functioning, exhibit a decline in elderly populations
(Hochanadel & Kaplan, 1984). Both the Wisconsin Card Sort
Test (WCST) and the Word Fluency Test-—each purported tests
of frontal lobe functioning--demonstrate a decline in
performance in older adults relative to younger adults

(Parkin & Lawrence, 1994). These neuropsychological tests

12

require the ability to monitor output, and flexibility to
generate different strategies and shift between strategies
efficiently. This constellation of abilities is subsumed
under the rubric of executive functioning (Shallice 1988;
Stuss & Benson, 1986). Older adults often make more errors
on tasks that involve executive functions relative to
younger adults, but also have difficulty inhibiting
incorrect responses and shifting strategies appropriately
(Parkin & Lawrence, 1994; Veroff, 1980). Parkin and
Lawrence found a significant correlation between performance
on the WCST and a recall and recognition task, suggesting
that the frontal lobes are involved in these facets of
memory. However, performance on a measure of verbal fluency
was not significantly correlated with memory performance.
Parkin and Lawrence's (1994) finding may be due to
differential sensitivity of the WCST and verbal fluency
tests to frontal lobe deficits. A study by Butler, Rorsman,
Hill and Tuma (1993) found that the verbal fluency task was
less sensitive to tumors in the frontal lobe than more
complex tasks. However, a significant deficit in verbal
fluency was demonstrated by subjects with both left frontal
lesions and bilateral frontal lesions (Benton, 1968; Perret,
1974). Furthermore, the analyses of verbal fluency
mentioned above, were constrained to the total number of
words produced. The executive functioning aspects of a
verbal fluency task include the ability to quickly generate

strategies, and to shift strategies when the current one is

13

no longer effective—both aspects which would be more
accurately measured by analysis of the order in which words
are produced. These findings illustrate the complex nature
of the relationship between the function of the frontal
system and performance on certain neuropsychological tests.

Further evidence for the involvement of the frontal
lobes in memory performance comes from studies of patients
with frontal lobe pathology. Gershberg and Shimamura (1995)
found that patients with frontal lobe damage were deficient
in both encoding and retrieval on a list learning task
relative to controls. The performance of older adults on a
list learning task was also evaluated in comparison with
patients with frontal lesions, in terms of strategic
functions and overall performance (Stuss, Craik, Sayer,
Franchi, & Alexander, 1996). Stuss and his colleagues found
that older adults demonstrated a modest impairment in list
learning, equivalent to that shown by patients with
unilateral right frontal lesions. Furthermore, when their
use of organizational strategies was evaluated, older adults
were deficient relative to younger adults and performed
equivalent to patients with unilateral right frontal lesions
(Stuss, et al., 1996). However, neither the older adults,
nor the frontal lobe lesion patients in the Stuss et a1.
study were impaired on tasks of primary memory such as digit
span, suggesting that the frontal lobes are primarily

involved in secondary memory deficits.

l4

However, caution must be used in making inferences from
studies of patients with pathology to the performance of the
able elderly. Although the performance of older adults on
certain neuropsychological tasks may resemble the
performance of those with pathology of the frontal system,
the elderly do not consistently demonstrate deficits in
social appropriateness as might be expected with such
impairment (LaRue, 1992).

Another consideration that must be made in the
evaluation of neuropsychological performance of the elderly
is the incidence of depression. Depression is considered
the second most common mental disorder in old age (LaRue,
1992). Although the percentage of older adults who meet the
criteria for major depression is low, the effects of mild to
severe depression can impact neuropsychological approach and
performance. Tasks that require attentional flexibility
reveal greater deficits for depressed elderly
subjects (Caine, 1981). Furthermore, memory tasks that
require more effortful processing for success are performed

poorly by depressed older adults (LaRue, 1992).

Verbal Fluency: Semantic and Phonemic Associations

 

The relationship between measures of executive
functioning and memory performance are complex and require
an analysis of the approach taken on the task, in order to
understand the relationship more clearly. However, most

studies have employed a quantitative approach in examining

15

the relationship between fluency tests and measures of
memory; that is, most studies have used the total number of
words produced, for analysis, while ignoring the production
strategies employed. Of particular interest to this study
is not only the performance demonstrated by older adults on
these fluency tests, but the manner of approach that is
employed by older adults in this task, and its potential
relationship to memory functioning and extent of executive
functioning deficits.

Perhaps the most rudimentary approach to a verbal
fluency task is a random generation of words as they come to
mind. However, given the constraints of this task—-
generating words that begin with a certain letter--the
random approach is typically least effective. Another
approach to a verbal fluency task utilizes associations
between words that rhyme or have similar sounds (e.g., fake,
flake or flake, flap) as well as utilizing associations
between words that belong to the same semantic category
(e.g., fun, frolic or apple, apricot). Associations based
on perceptual or sound characteristics of words represents
phonemic associations, while associations based on meaning
of words represents semantic associations. Hochanadel and
Kaplan (1984) reported that in clinical observation,
subjects with frontal system impairment not only produced
fewer words, but tended to demonstrate reliance on a
phonemic strategy; that is, they were more likely to use

associations between the perceptual and pronunciation

16

characteristics of words, such as "flake" and "flap" when
trying to generate as many words as possible that begin with
a certain letter. While empirical validation of this
observation has not yet been achieved, a study by Raskin,
Sliwinski, and Borod (1992) found that patients with
Parkinson's Disease were impaired in their ability to use
semantic clusters on a verbal fluency task compared to
normal controls. Most studies employing verbal fluency
measures have focused on the quantity of words produced,
while ignoring

the production strategy that is being used by older adults.

Performance on verbal fluency tests should be greatest
when subjects are able to shift between using semantic
associations to phonemic associations and back again
quickly. The demand of the verbal fluency task for shifting
between strategies requires spontaneous flexibility for
greatest performance, and is similar to demand of the WCST
for shifting strategies. Analysis of this aspect of the
verbal fluency test in relation to performance on the WCST
should elucidate the relationship between these two measures
of frontal lobe functioning.

Furthermore, the relationship between tests of verbal
fluency and memory functioning may be made clearer by
analysis of the association strategies utilized by older
adults in production of words on a verbal fluency test and
the encoding process of forming associations between words

on a memory test. The deficiency in using a semantic

17

association strategy on the verbal fluency test and
preference for phonemic production strategies may be
reflective of an overall decline in the depth of information
processing engaged in by older adults, due in part to
frontal lobe deterioration. Although, the elderly are
capable of utilizing and forming associations between words,
they typically do not engage in this type of effortful
encoding process on memory tasks (Craik & Byrd, 1982).

Light and Burke (1988) found a larger age difference in
older adults' ability to form associations between weakly
related events than between strongly related events, and
that in general, the elderly have more difficulty forming
new connections in memory. On a verbal fluency task, a
deficiency in depth of processing would be represented by
the difficulty older adults have in utilizing the semantic
associations of words, while relying on the more surface
level phonemic associations, or a random production strategy
to generate words. This failure to engage in more effortful
processing on a verbal fluency task may be related to the
decline in effortful encoding processing used on memory
tasks by older adults. Furthermore, when an analysis of the
production strategy used on the verbal fluency task is done,
the relationship between this executive function task and

strategy use on a memory task may be more clear.

18

Aims of Current Study

 

The aim of this study is to investigate the
relationship between the ability of older adults to shift
strategies on a verbal fluency task and their ability to
shift strategies on another task of executive function.
Performance on the verbal fluency task should be greatest
when the elderly are quickly able to produce all of the
words that are associated either phonemically or
semantically and quickly shift when a particular association
is no longer productive. This ability should be related to
the ability of older adults to shift from a sorting strategy
that is no longer correct to another sorting strategy, using
tests designed to assess attentional flexibility (e.g.
Wisconsin Card Sort Test).

Furthermore, an investigation of the relationship
between the ability of older adults to generate and shift
between strategies on a verbal fluency task -— as evidenced
by the incorporation of semantic associations between words
-- and the ability to use semantic associations between
words on a memory task, is an additional aim of this study.
Although older adults are capable of utilizing semantic
information when encoding information to be remembered, they
do not spontaneously do so (Craik & Byrd, 1982). Rather,
the elderly tend to use less effortful encoding strategies
such as phonemic characteristics of words to be learned.
Light and Burke (1988) suggested that older adults were

impaired in their ability to form new associations on a

19

memory task, and that they were more likely to use the most
readily available information during encoding rather than
generating novel strategies.

An analysis of the strategies used on a verbal fluency
task requires that the clusters of words produced be
examined as to their relationship. Whenever two successive
words are produced that share the same second phoneme such
as "fork" and "form" or two successive words rhyme, such as
"flake" and "fake" is considered a phonemic cluster.
Semantic clusters consist of two consecutive words that
share a semantic category such as "apple" and "apricot" or
are similar forms of a word such as "fun" and "frolic".
Analysis of the pattern of phonemic clusters and semantic
clusters are of particular value in evaluating the
relationship between performance on a verbal fluency task
and performance on the WCST, another task of executive
functioning. Specifically, it is the hypothesis of this
study that limited word production on a verbal fluency task,
dominated by a random (no associations) strategy or reliance
on phonemic associations, will predict lower performance on
the WCST. This finding would demonstrate that one aspect of
executive functioning that is assessed by both a verbal
fluency task and the WCST is attentional flexibility,
demonstrated by the ability to shift strategies when one is
no longer effective. Verbal fluency tasks as they are
typically utilized (analyzing total number of words

produced) may not be particularly sensitive to frontal lobe

20

functioning (Butler, Rorsman, Hill, & Tuma, 1993). However,
if verbal fluency tasks are analyzed as a measure of
attentional flexibility, their utility in detecting the
executive functions of the frontal lobe may be improved.
Furthermore, the use of phonemic and semantic clusters
is of interest for the examination of the relationship
between performance on a verbal fluency task and performance
on a memory task. It is the hypothesis of this study that
the ability of older adults to generate more elaborate
strategies on a verbal fluency task, demonstrated by
utilization of semantic associations will be related to the
ability to generate more elaborate encoding strategies on a
memory task (e.g. California Verbal Learning Test) as
evidenced by utilization of semantic categories. That is,
word production on a fluency task, dominated by a random or
a phonemic association strategy, will predict a reduced
ability to utilize the semantic characteristics to cluster
items during encoding on a memory task. If this is found it
will provide evidence for the relationship between the
executive functions (specifically, attentional flexibility)
of the frontal lobe and age related memory decline. More
specifically, the more intact an individual's frontal lobe
functioning, as measured by the ability to spontaneously use
a variety of effortful associations on a verbal fluency
task, the more likely they will spontaneously engage in

effortful strategies on a memory task.

21

To summarize, the hypotheses are:

Hypothesis 1. Total number of words produced by semantic

 

associations on a verbal fluency task will be positively
correlated with use of semantic clusters during recall on a

new learning task (i.e. CVLT, observed semantic clusters).

Hypothesis 1a. The use of semantic associations on a verbal

 

fluency task is indicative of executive functioning and will
predict the use of semantic encoding on the CVLT, (as

evidenced by the use of semantic clusters during recall).

Hypothesis 2. The use of a semantic association strategy on

 

a verbal fluency task, will be negatively correlated with
perseverative errors on the WCST. Perseverative errors on
the WCST are indicative of a failure to shift strategy in
response to feedback, and should be negatively correlated
with semantic associations used on a verbal fluency task if
these associations are the best indicator of executive

function, specifically attentional flexibility.

Hypothesis 3. Increased depression scores as measured by

 

the GDS will be negatively correlated with total strategy
(total number of phonemic, semantic and random association

clusters) use on a verbal fluency task.

METHODS

Participants

 

Seventy older adults (over age 55) were recruited from

the East Lansing and Lansing communities, through newspaper

22

advertisements to participate in the ongoing Michigan State
University (MSU) Psychological Clinic Aging Research
Project. Each individual was offered assessments of their
mood and memory, as well as a seven-session workshop
designed to teach relaxation and cognitive strategies for
the relief of depression and / or memory difficulties. From
these respondents, 62 older individuals ranging from 55 to
90 years of age (M = 67.13; SD = 8.10) were included in the
analysis. These 70 participants (51 Women and 19 men), with
a mean education of 14.7 (SD =2.5) were screened for
depression, mental status, and a range of health problems to
rule out the effects these might have on mental functioning
and subsequent performance on the administered
neuropsychological measures. Individuals with severe
depression, as determined by scores of 20 or higher on the
GDS were referred elsewhere for treatment. Furthermore,
individuals scores lower than 25 on the MMSE were not
included in the analysis. Eight participants were dropped
from the analysis for MMSE scores lower than 25. No other

data was trimmed.

Measures

a. Geriatric Depression Scale (GDS; Yesavage & Brink, 1983)
The GDS was used to asses the depression of

participants in the study. This scale was specifically

designed for rating depression in the elderly. The GDS is

composed of 30 true/false self-referent statements.

Yesavage and Brink (1983) found a positive correlation

23

between conventional cutoffs and selected diagnosis
Classifications of the Research Diagnostic Criteria for
definition of major and minor depressive disorders.
Furthermore, test-retest reliability was found to be .85
over a two week time frame, suggesting that the GDS
reflected stable individual differences. Convergent
validity was found between the GDS and the Zung Self-Rating
Scale for Depression and the Hamilton Rating Scale for
Depression as .84 and .83 respectively.

b Mini Mental State Exam.(MMSE; Folstein, Folstein, &
McHough, 1975)

The MMSE is a measure of orientation that has received
extensive use in determining gross cognitive functioning.
This test requires memory ability, orientation, and the
ability to follow commands. When subjects were evaluated
over a 24-hour period
test-retest reliability was between .85 to .99. The
standardization sample of the MMSE consisted of 63 healthy
elderly control subjects (mean age 74). Control subjects'
scores were in the range of 24.6 to 27.6, while demented
subjects scored between 9.6 t012.2. A cut-off score of 25
is often applied to discriminate scores more suggestive of
impairment. The MMSE was used to rule out dementia in the
participants of this study.

(L Measures of Executive Functioning

Controlled Oral Word Association Test (FAS; Benton &
Hamsher, 1977)

24

The FAS requires subjects to produce as many different
words as possible that begin with a letter of the alphabet
(F, A, and S) excluding proper nouns in 60 seconds.
Subjects are also instructed that variations of the same
root word (e.g. book, bookworm) are not permissible.
Responses are recorded verbatim and words that meet the
above criteria are included in the total score. Proper
nouns and words that are repeated are scored as
perseverations. In addition to this quantitative scoring of
the FAS, the production strategies of older adults was also
of interest for this study. Phonemic clusters were defined
as two successive words with the same second phoneme (e.g.
fork, form) or two successive words which rhyme (e.g. flake,
fake). Semantic clusters included any two words that share
a semantic category (e.g. apple, apricot) or were similar
forms of a word (e.g. fun, frolic). Total number of words
produced by phonemic association clusters and semantic
association clusters to total word production were computed
for the purpose of comparison. Two independent raters were
used to determine the number of words produced by phonemic,
semantic and random association strategies. One-year retest
reliability in older adults has been reported as .70 (Snow
et. al., 1988). Concurrent validity has also been
established for the FAS (Coelho, 1984).
Wisconsin Card Sorting Test (WCST; Heaton, 1981)

The WCST requires subjects to sort stimulus cards when

they are not given any instructions as to the sorting

25

principles, which change during the task. Feedback is
given, as to whether the response was right or wrong, but
the sorting principles are never revealed. Perseverations
on this test are demonstrated by using the sorting principle
from a previous category, repeatedly after the principle has
changed. Generalizability coefficients, which reflect the
fidelity of true-score measurement, and can be viewed as
analogues of traditional reliability coefficients (according
to Heaton, 1981) were calculated and averaged .57 with a
median of .60, based on a single test administration. The
WCST has demonstrated good construct validity for use with
the elderly (Paolo, Troster, Axelrod, & Koller 1995). Good
support was found for a general conceptualization/problem
solving factor and for a failure to maintain set component.
Both of these factors subsume several aspects of frontal
system functioning.

d. California Verbal Learning Test (CVLT; Delis, Kramer,
Kaplan, & Ober, 1987)

The CVLT is a learning task which assesses verbal
learning and memory. The CVLT measures the immediate, short
delay, cued, long delay and free recall of presented
information. The CVLT was developed to go beyond traditional
memory tests, and quantify additional indices such as
semantic clustering and perseveration rates. The CVLT
requires subjects to remember 16 items that belong to four
semantic categories. The normative sample found test-retest

reliability was .59 on the CVLT; further analyses of the

26

normative sample have cited a coefficient alpha of .74 and
split—half reliability as .63. Criterion-related validity
of the CVLT has been demonstrated by its correlation with
the Wechsler Memory Scale, Memory Quotient of .66. Factor
analysis studies have supported the utility of the component
factors of the CVLT (Delis, Freeland, Kramer & Kaplan,

1988).

RESULTS

Individuals with scores lower than 25 on the MMSE were
not included in the analysis. Eight participants were
dropped from the analysis for MMSE scores lower than 25,
resulting in a final N of 62. No other data was trimmed.
Two independent raters were recruited to calculate the
number of semantic, phonemic and random clusters of the
participants on a verbal fluency test. Semantic clusters
were defined as any two consecutive words that shared a
semantic category such as "apple" and "apricot" or were
similar forms of a word such as "fun" and "frolic". Phonemic
clusters were defined as any two successive words that
shared the same second phoneme such as "fork" and "form" or
two successive words rhyme, such as "flake" and "fake".
Random clusters were defined as any two consecutive words
that did not meet criteria for being a phonemic or semantic
cluster. A reliability coefficient alpha of .92 was
achieved by the independent raters for semantic clusters.
Random and phonemic clusters achieved a reliability

coefficient alpha of .90 and .99 respectively, but were

27

not used in the analyses. The independent ratings for
semantic clusters were averaged for the purposes of
analysis.

The averaged semantic clusters ranged from 0 to 6 (M
1.73, SD i1.49). The observed semantic clusters on the CVLT
ranged from 4 to 76 (M 26.29, SD 115.71). Perseverative
errors on the WCST ranged from 3 to 54 (M 20, SD 118.32).
The total number of depressive symptoms endorsed on the GDS
ranged from 0 to 29 (M 7, SD 16.47).

Hypothesis 1. Total number of words produced by semantic
associations on a verbal fluency task will be positively

correlated with use of semantic clusters during recall on a
new learning task (i.e. CVLT, observed semantic clusters).

 

It was predicted that the total number of words
produced by semantic associations on a verbal fluency task
would be positively correlated with use of semantic clusters
during recall on a new learning task. This hypothesis was
supported. A one-tailed Pearson correlation coefficient was
calculated between the average of the total semantic
clusters used on a verbal fluency task and the total number
of observed semantic clusters on the CVLT and was found to
be significant (r = .23, p<.05) indicating that these two
variables are positively related.

Hypothesis 1a. The use of semantic associations on a verbal
fluency task is indicative of executive functioning and will

predict the use of semantic encoding on the CVLT, (as
evidenced by the use of semantic clusters during recall).

 

It was also expected that use of semantic associations

on a verbal fluency task would be indicative of executive

28

functioning and would predict use of semantic encoding on
the CVLT. This hypothesis was supported. A linear
regression was conducted to determine if semantic clusters
used during recall on a new learning test (i.e., CVLT,
observed semantic clusters) was predicted by total number of
words produced by semantic associations on a verbal fluency
task. The Beta coefficient for the semantic associations on
a verbal fluency task indicated that these associations are
a significant predictor of semantic clustering strategy on
the CVLT (Beta = 2.62 ; p<.05).

Hypothesis 2. The use of a semantic association strategy on
a verbal fluency task, will be negatively correlated with
perseverative errors on the WCST. Perseverative errors on
the WCST are indicative of a failure to shift strategy in
response to feedback, and should be negatively correlated
with semantic associations used on a verbal fluency task if

these associations are the best indicator of executive
function, specifically attentional flexibility.

 

Use of a semantic association strategy on a verbal
fluency task was expected to be correlated positively with
perseverative errors on the WCST, as perseverative errors on
this task indicate a failure to shift strategies in response
to feedback. This hypothesis was not supported. A one-
tailed Pearson correlation coefficient was conducted between
the total semantic clusters used on a verbal fluency task
and the perseverative errors made on the WCST and was found
to be non-significant (r = .08 ; ns).

Hypothesis 3. Increased depression scores as measured by
the GDS will be negatively correlated with total strategy

(total number of phonemic, semantic and random association
clusters) use on a verbal fluency task.

 

29

Finally, it was predicted that increased depression
scores as measured by the GDS would be negatively correlated
with the total number of strategies used on a verbal fluency
task. This hypothesis was not supported. A one-tailed
Pearson correlation coefficient was conducted between the
total number of association clusters used on the verbal
fluency task and the total GDS score and was not found to be

significant (r = .09; ns).

DISCUSSION

The first hypothesis of this study was that the total
number of words produced by semantic associations on a
verbal fluency task would be positively correlated with use
of semantic clusters during recall on a new learning task.
This hypothesis received empirical support. Furthermore,
this finding suggests that the degree to which healthy older
adults are able to generate words quickly (on the verbal
fluency test) is related to the ability to use strategies
when presented with unorganized verbal material that is to
be learned. The foregoing results suggest that there is
utility in examining the approach to studying
neuropsychological tests in a more qualitative manner.
Verbal fluency tasks require the participant to generate as
many words as possible that begin with a certain letter,
within a constrained amount of time. In order to maximize
performance, effective word retrieval strategies must be
readily activated. The use of a semantic association

strategy on a verbal fluency task is a more complex means of

30

retrieving words than is using phonological aspects (i.e.
rhyming or similar sounds). A study by Parks and his
colleagues (1988) of metabolic activation during a verbal
fluency task found that participants who performed well
exhibited lower metabolic activation than those who
performed poorly. It has been suggested by Parks et al.,
that this reduced activation was indicative of an increased
availability of efficient strategies, which required less
metabolic activation. However, no distinction between what
constitutes efficient strategies was made in this study.
Furthermore, the speculation that efficient strategies
require less metabolic activation requires further empirical
study.

The second part of the first hypothesis was that the
semantic associations used on a verbal fluency task were
indicative of executive functioning and would predict use of
semantic encoding on the CVLT. This hypothesis was
supported and implicates the involvement of the frontal
lobes, as the mediator of executive functions, in the
process of strategy generation for both of these tasks (CVLT
and verbal fluency). The relationship between the frontal
lobes and strategy generation has been supported by
additional research. Parks et al. (1988) found that
although several cerebral structures were activated during a
verbal fluency task, participants with left frontal damage
had poor performance. Additionally, a study by Mangels

(1996) implicated the involvement of the frontal lobes in

31

memory retrieval. Patients with frontal lobe lesions were
impaired in recall for remote information and were not aided
by the provision of semantic or phonemic cues.

Additional evidence for the involvement of the frontal
lobes in age-consistent memory decline, through a decrement
in strategy use was found by Stuss et al., (1996). Stuss
and his colleagues found that older adults show impairment
on learning lists that are unorganized. Furthermore, the
poor use of organizational strategies employed by older
adults were similar to the use of these strategies by
patients with unilateral frontal lobe lesions. Eslinger and
Grattan (1994) found that organizational abilities in memory
are affected in frontal lesions although not from lesions to
other cortical areas. Spontaneous flexibility is similarly
disturbed in patients with frontal lobe lesions; suggesting
that spontaneous flexibility and memory organization
abilities are related mediated through the frontal lobes
(Eslinger & Grattan, 1994). This finding seems to be
supported by the current findings. A question which still
needs investigation is whether or not data from brain
impaired individuals is applicable to individuals with
“normal” brains.

The second hypothesis of the present study was that
failure to shift strategies in response to feedback on the
WCST would be negatively correlated with semantic
associations used on a verbal fluency task. This hypothesis

was not supported as using a semantic association strategy

32

was not negatively correlated with perseverative errors on
the WCST. Both verbal fluency and the WCST involve
executive functions of the frontal lobe and would be
expected to be correlated. Although the frontal lobe has
been implicated in the performance of verbal fluency tasks
as well as the WCST (Parks, et al., 1988; Anderson, Damasio,
Jones & Tranel, 1991) there has been some research
suggesting that performance on either task alone is not
predictive of frontal lobe dysfunction (Butler, Rorsman,
Hill, & Tuma, 1993; Robinson, Heaton, Lehman, & Stilson,
1980).

Verbal fluency and the WCST require executive functions
that have been labeled cognitive flexibility; that is, the
ability to shift avenues of thought and process information
in a variety of ways (Eslinger & Grattan, 1993). Eslinger
and Grattan distinguished between verbal fluency and the
WCST as representing spontaneous flexibility and reactive
flexibility measures, respectively. Verbal fluency is more
dependent on the ability to generate a diversity of
strategies, and switch quickly among them, based on internal
perceptions of the effectiveness of a particular strategy
for generating more words. On the other hand, the WCST
requires readiness to freely shift strategies in response to
explicit feedback. Eslinger and Grattan found that while
both spontaneous flexibility and reactive flexibility were
similarly impaired in patients with frontal lobe and basal

ganglia damage, spontaneous flexibility tasks were markedly

33

disturbed by frontal lobe damage. The findings of the
current study seem to support this distinction between the
types of cognitive flexibility measured by these two tasks.
Given the findings of Eslinger and Grattan, the finding of
this study that a measure of the strategies used on a verbal
fluency task and the ability to shift strategies in response
to explicit feedback on the WCST is not surprising.

The frontal lobe has similarly been implicated in
normal age-consistent memory loss (Parkin & Lawrence, 1994;
Stuss et al., 1996). However, the relationship between the
frontal lobes and memory performance in older adults has
been largely dependent on the aspect and type of memory
(e.g., recall vs. recognition; episodic vs. verbal) being
considered (Tulving, Kapur, Craik, Moscovitcch, & Houle,
1994; Kapur et al., 1994). It may be of interest in a
follow-up study to use the WCST and verbal fluency task to
determine if these tests are capable of dissociating
different memory functions on a learning task such as the
CVLT. Specifically, if the WCST perseverative error score
is related to the ability to shift strategies in response to
explicit feedback, that score should be associated with the
ability to use semantic categories on the CVLT after a
delay, when the categories are provided prior to the delay.

Finally, the third hypothesis of this study was that
depression would be negatively correlated with use of
strategies on a verbal fluency task. This hypothesis was

not supported. Given the finding that tasks requiring

34

attentional flexibility reveal greater deficits in depressed
elderly subjects (Caine, 1981) the finding of the current
study is somewhat surprising. However, the sample of the
present study does not include a large number of subjects
who would qualify as more than mildly depressed. Indeed,
the mean score on the GDS for the sample (M 7, SD i6.47)
falls in the normal range (Yesavage & Brink, 1983).
Furthermore, the GDS consists of a variety of symptoms
related to depression. A more specific analysis of items
that pertain to symptoms of depression, such as a loss of
energy, may be more related to effort expended in the
generation of strategies

However, some caution in interpreting the current
findings is warranted due to methodological limitations of
the current study. Despite the evidence from previous
research implicating the frontal lobe in the memory process
of encoding, and in generating words on a fluency task, no
neuroimaging was conducted in this study; therefore, no
conclusions can be made as to the specific neuroanatomical
location of these functions. However, both the generation
of strategies during a learning task and a verbal fluency
task seem to be functionally related.

Furthermore, there has been some research that has
found that gender and verbal intelligence account for a
significant portion of the variance in FAS performance,
although they found that level of education was unrelated

(Bolla, Lindgren, Bonaccorsy, & Bleecker, 1990). It has

35

also been suggested that verbal fluency is a measure of IQ
as opposed to a measure of frontal lobe functioning (Miller,
1984). Neither of these variables were accounted for in the
present study as both men and women were included in the
analysis. However, the participants in the present sample
consisted of a highly educated group with a high level of
verbal intelligence as estimated by the AMNART (M=115, SD
116.57). It is also important to note that the study by
Bolla et al., was principally concerned with total number of
words produced on a verbal fluency task and did not analyze
the strategies employed.

Similar to the finding of Bolla et al. (1990), Veroff
(1980) found a significant difference in the performance of
males and females on a verbal fluency task. However,
neither study examined differences in production strategies
on this task. Furthermore, when the influence of gender was
factored out the correlation between semantic clusters and
use of semantic encoding strategies was close for both men
and women. In the present study the following results were
obtained when the effect of gender was partialled out for
men (N=18; r = .20) and for women (N=44; r = .18).

One alternative explanation of the current findings in
regard to a deficit in using effective strategies at
encoding has been proposed by Salthouse (1982) as a
generalized slowing of processing speed that is consistent
with normal aging. Salthouse (1993) found that when the

effects of perceptual speed were partialled out, age-related

36

effects on memory performance accounted for only a small
proportion of the variance. The finding of this study that a
relationship between generation of strategies on a verbal
fluency task and a memory task exists may be due to a
generalized slowing of processing in older adults, rather
than to the hypothesized decrease in efficiency of frontal
lobe functioning. Although Salthouse has found support for
the influence of processing on memory performance, the
mechanism through which this influence is mediated is still
open to speculation.

It is possible that reduced efficiency of executive
functions of the frontal lobes is a consequence of normal
aging and responsible for reductions in processing speed.
However, this question can not be addressed by the current
study. The measure of verbal fluency used in this study
requires the quick generation of strategies to produce as
many words as possible in one minute. It may be that the
performance of older adults on this task would demonstrate
an increased use of strategies if an unlimited or extended
amount of time was provided to accommodate reductions in
processing speed. Furthermore, the CVLT does not restrict
time allowed for immediate recall, however, the words to be
learned are presented at a rate of approximately one per
second. It is possible that the deficit in use of efficient
encoding strategies demonstrated by older adults is due to a
reduction in processing speed, rather than in a deficit of

an executive function such as strategy generation.

37

It is also important to note that no normative data
exist on strategies used on a verbal fluency task.
Furthermore, no study was done with younger adults to
determine if they are more likely to use elaborate
strategies on a verbal fluency task such as semantic
clustering; therefore, it can not be determined from the
present study if subtle deterioration of the frontal lobes
is responsible for the detriment in strategy use on verbal
fluency and memory tasks by older adults. It would be
interesting to determine the extent to which the decline in
verbal fluency in older adults is due to an age-consistent
reduction in strategy generation.

Collecting normative data on strategy use on a verbal
fluency task throughout the lifespan would be instrumental
to providing additional support to the findings of a
decrease in this particular executive function in older
adults. Furthermore, neuroimaging data may be able to make
clear the relationship between generating strategies on a
verbal fluency task and generating strategies on a memory
task, and provide more specific localization information in
regard to these abilities.

Finally, the role of different types of cognitive
flexibility in memory functioning could be elucidated by
further analyses of the WCST and the CVLT. Specifically, it
was found in this study that the shifting of strategies in
response to explicit feedback on the WCST was not related to

shifting of strategies on a verbal fluency task, despite

38

both of these tests supposed reliance on frontal lobe
functioning. However the distinction made by Eslinger and
Grattan (1993) of spontaneous flexibility and reactive
flexibility as functions assessed by verbal fluency tasks
and the WCST respectively, may be of use in discriminating
the role of these executive functions in memory performance.
The CVLT presents an unorganized list of items five times,
followed by a cued recall trial after a short delay.
Approximately 20 minutes after this cued recall, a free
recall trial is administered. If an increased use of
semantic strategies was demonstrated during this long-delay
free recall, this should be related to WCST perseverative
errors, as these are an index of incorporating feedback to
use different strategies.

Further research is needed to elucidate the importance
of the current findings. Normative data on the patterns of
strategy use throughout the lifespan needs to be collected,
in order to make any comparative remarks about the process
of normal aging on strategy generation. Additional
neuroimaging studies similar to those undertaken by Parks et
al. (1988) which separate types of strategies used, may
provide further understanding of the localization of
strategy generation on both verbal fluency tasks and memory
tasks. Furthermore, studies of the frontal lobes
involvement in tasks of executive functions such as
spontaneous and reactive flexibility, and the role of those

functions in memory remain to be conducted.

39

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