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Neuropsychological Rehabilitation

An International Journal

ISSN: (Print) (Online) Journal homepage: https://www.tandfonline.com/loi/pnrh20

Effects of working memory intervention on


language production by individuals with dementia

Mi Sook Lee & Bo Seon Kim

To cite this article: Mi Sook Lee & Bo Seon Kim (2020): Effects of working memory intervention
on language production by individuals with dementia, Neuropsychological Rehabilitation, DOI:
10.1080/09602011.2020.1789479

To link to this article: https://doi.org/10.1080/09602011.2020.1789479

Published online: 17 Jul 2020.

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NEUROPSYCHOLOGICAL REHABILITATION
https://doi.org/10.1080/09602011.2020.1789479

Effects of working memory intervention on language


production by individuals with dementia
Mi Sook Leea and Bo Seon Kim b

a
Department of Audiology and Speech-Language Pathology, Hallym University of Graduate Studies,
HUGS Center for Hearing and Speech Research, Seoul, Korea; bSeoul Asan Rehabilitation Clinic,
Incheon, Korea

ABSTRACT ARTICLE HISTORY


The purpose of this study was to investigate the effects of Received 16 August 2019
working memory intervention on language production by Accepted 19 June 2020
people with mild or moderate Alzheimer’s disease (AD). A
KEYWORDS
total of 39 AD patients, 21 with mild AD and 18 with Working memory
moderate AD and 18 normal controls were given 18 intervention; language
sessions of working memory intervention. After these production; Alzheimer’s
sessions, the transfer effects and maintenance effects at the disease; transfer effect;
3-month follow-up were assessed. A word-span task and a maintenance effect
digit-span task were used to evaluate working memory.
Language-production abilities were compared through four
tasks: a verbal fluency, a confrontation naming, a word
definition, and a picture-description task. Task performances
of working memory and language production were the
lowest in the baseline stage and the highest in the transfer-
effect stage. The three groups had transfer effects in all
tasks, while the maintenance effects were limited by groups
and tasks. This study proves that working memory
intervention for AD patients is effective for language
production. In addition, we have paved the way for working
memory intervention to improve language production by
AD patients in clinical settings by presenting the transfer
and maintenance effect for each task of language production.

Working memory (WM) is the ability to hold information while performing the
various tasks of everyday life; it is involved in the short-term storage and manipu-
lation of information (Peach & Shapiro, 2012). A multi-component system, WM
has limited capacity to store information temporarily or to distribute attention
among processes. WM is also directly related to executive functioning, including
the allocation of attention to information and the selection, inhibition, and
updating of information (Lezak et al., 2004).
WM and executive functions are dominated by the prefrontal cortex and the
nigrostriatal dopamine neurotransmitter system (Raz, 2005; Volkow et al., 2000).
Both areas are sensitive to neurological changes, such as aging and neurological

CONTACT Bo Seon Kim bskimslp@gmail.com Seoul Asan Rehabilitation Clinic, 818 Hogupo-ro, Namdong-
gu, Incheon 21534, Korea
© 2020 Informa UK Limited, trading as Taylor & Francis Group
2 M. S. LEE AND B. S. KIM

disorders (Dennis & Cabeza, 2008; Raz, 2005). These changes are more active in
the prefrontal cortex as neurons contract and the density of synapses decreases.
In addition, as the interneuronal signalling changes or adjusts, the relationship
between stimuli and responses can be altered and the sensitivity to stimuli
can be reduced (Li, 2005; Li et al., 2000).
WM is impaired from the early stages of mild cognitive impairment (MCI) or
Alzheimer’s disease (AD) due to these neurological changes (Huntley &
Howard, 2010; Missonnier et al., 2007; Rosen et al., 2002). The deficits in WM
caused by AD bring on difficulties in performing tasks in daily life. In particular,
executive control of WM sensitively reflects the progress of AD (Belleville et al.,
2007). Strategic encoding of information is crucial to the performance and learn-
ing of WM, which is damaged even at the earliest stages of AD (Huntley et al.,
2011). Components of WM associated with executive functions are also key pre-
dictors of MCI-to-AD progress (Saunders & Summers, 2011).
The deficits in WM cause impairments in language and communication skills.
For example, if reading and listening span tasks are poorly performed, the per-
formance of reading and listening comprehension and reading, learning, and
computing abilities also decline (Hitch et al., 2001). The lower the WM (Borella
et al., 2008), the poorer the language processing ability, and the deficits in
WM seen in MCI or AD patients negatively affect the understanding of the
meaning and form of complex syntax (Bier et al., 2008; Kemper et al., 2001;
Waters & Caplan, 2001).
Decreased WM degrades language production as well as language compre-
hension. MCI patients who show deficits in WM have difficulty with the repetition
of complicated sentences or with verbal-fluency tasks because the process of
manipulating and processing input information is reduced (Lee & Kim, 2019;
Waters & Caplan, 2001). There is also a strong correlation between span tasks
and the fluency, grammatical complexity, and content of spontaneous speech
(Peach & Shapiro, 2012). Many studies have identified the association between
WM and verbal abilities and verbal fluency through the analysis of spontaneous
speech (Dennis & Cabeza, 2008; Kemper & Sumner, 2001; McDowd et al., 2011).
For example, AD patients are overly reliant on stereotypes, empirical knowledge,
and heuristics, as well as schemas that have already been learned, due to the
deterioration of WM and executive function, which results in lower phonemic
and semantic verbal fluency and confrontation-naming abilities (Lee & Kim,
2019; Peach & Shapiro, 2012).
Word-definition ability reflects semantic language expression at the sentence
level and requires a complex combination of semantic processing ability, cogni-
tive function, and semantic knowledge of objects (Hough, 2007). Consequently,
deficits in WM due to neurological changes have a negative impact on word-
definition ability. In other words, if WM is degraded, words and related semantic
features stored in a semantic network cannot be processed or generated with
rapidity and precision (Chow et al., 2006; Troyer, 2000).
NEUROPSYCHOLOGICAL REHABILITATION 3

In the case of language tasks, which present a number of nouns and types of
verbs differently, the lower the WM is, the higher the error rate is (Kemper et al.,
2003). In addition, individuals with poor WM used shorter sentences, lower sen-
tential complexity, and less information. A discourse production task, which
reflects the semantic, syntactic, and pragmatic abilities of language, sensitively
reflects deficits in WM due to neurological changes (Borella et al., 2008). In par-
ticular, as WM decreases, the appropriateness of information delivery and the
efficiency of communication are lowered (Kim & Lee, 2019a; March et al.,
2009). In the analysis of spontaneous speech of the elderly and AD patients by
Kemper et al. (2001), the syntactic complexity and the content of propositions
were lowest for the mid-70s, and AD patients continued to decline regardless
of age.
As the relationship between WM and other cognitive-language abilities is
demonstrated, the discussion about gains from WM intervention is becoming
more active. The effect of WM intervention for the elderly is mainly reflected
directly in the WM capacity (Carretti et al., 2012; Richmond et al., 2011). There
is also a transfer effect of intervention in the mechanism associated with WM,
such as inhibition or processing speed and in the cognitive processing based
on WM, such as fluid intelligence or language comprehension (Borella et al.,
2010; Carretti et al., 2012). In fact, a study on amnestic MCI has shown that train-
ing of verbal WM had a transfer effect to visual memory, fluid intelligence, and
long-term memory (Carretti et al., 2013).
Further, the paradigm of WM intervention has an effect on language abilities
(Lee & Kim, 2020). Based on the processing, there is a multistore model in which
WM is processed in a temporary area, separate from long-term memory, and a
unitary store model in which all information is collected in one memory
system (Nee et al., 2008). According to these theories, the applicable intervention
paradigm varies. The method of intervention differs depending on the view of
the WM capacity as the number of slots that can be used for memory and the
view of the capacity itself. In general, considering the WM intervention paradigm,
it is often based on domain-general or executive elements and domain-specific
elements (Lee & Kim, 2020). They are all involved in linking WM with higher
dimensional cognition and language (Kane et al., 2004). The domain-general
elements are processed independently from a specific type of information or
sensory modalities, support encoding, retention, and retrieval of information
from WM. Further, these elements control attention, transmit information in
and out of WM buffers, and reduce interference from irrelevant sources.
However, domain-specific elements associated with detailed strategies are
involved in retaining and handling certain types of information (Morrison &
Chein, 2011). The core training (CT) paradigm is based on the domain-general
WM mechanism, and the strategy training (ST) paradigm aims to increase the
performance of tasks that require the retention of information (Morrison &
Chein, 2011). CT combines various components of the WM system with stimulus
4 M. S. LEE AND B. S. KIM

types, and thus has a large transfer effect, especially in reading comprehension,
cognitive control, reasoning, and anecdotal memory (Chein & Morrison, 2010).
Although ST has been proven to be functionally effective in terms of using every-
day contexts (Carretti et al., 2007), its dependence on a specific memory strategy
is high, and only the near transfer effect limited to training tasks is reported (St
Clair-Thompson et al., 2010).
For effective WM intervention, the difficulty and load of tasks should also be
considered, and their manipulation should be consistent (Borella et al., 2010; Car-
retti et al., 2012). By doing so, it is possible to handle coding, information reten-
tion, suppression of irrelevant information, simultaneous execution of dual tasks,
and attention control, and to facilitate fluid approaches to tasks. The improve-
ment of WM capacity through intervention and transfer to other cognitive-
language abilities demonstrates that some degree of brain plasticity is preserved
after aging or neurological disease (Carretti et al., 2013). In other words, WM
intervention can produce a structure that compensates for neurological
changes (Borella et al., 2010). Therefore, WM intervention for MCI or AD patients
is essential in that it promotes a compensatory mechanism (Bokde et al., 2010).
The effects of WM intervention on language skills are often limited to
language comprehension. In Carretti et al. (2012), the ability of language compre-
hension of the elderly who received WM training was greatly improved, and their
performance was maintained even after 6 months. A person with a low reading
span has a poor ability to interpret and maintain various ambiguous phrases
(Just & Varma, 2002), and it is necessary to take this into account when training
WM. Tasks that recall or utilize information (such as answering questions or
matching sentences and pictures) tend to reinforce the processing of infor-
mation in the memory (Peach & Shapiro, 2012). WM intervention is reported
to improve the accuracy of phonological awareness and word recall among
the elderly (Nittrouer et al., 2016), and calculation abilities and language compre-
hension of AD were also improved (Cowan, 2005).
However, studies focusing on the effects of WM intervention on language pro-
duction are scarce. One study has shown that older adults have improved verbal
fluency and sentence memory due to WM intervention using a home-based
computer programme (Payne & Stine-Morrow, 2017). A WM intervention using
verbs in aphasic patients improved verbal fluency and the production of
target verbs and untrained verbs (Edmonds & Babb, 2011).
A further study noted that planning for sentence production is highly related
to verbal WM (Nittrouer et al., 2016). In other words, to improve the efficiency of
planning at the phonological level, verbal WM should be supported, reflecting
the overlap of the resources allocated for phonological planning in language
production and verbal WM. There is also the suggestion that language-specific
tasks, such as poetry-based stimulation, should be combined with WM training
to improve expressive language abilities, such as verbal fluency and discourse
production (Zimmermann et al., 2014). According to Lee and Kim (2020) who
NEUROPSYCHOLOGICAL REHABILITATION 5

examined the effect of the type of WM intervention on language production


ability, the application of the domain-general intervention to mild to moderate
AD patients significantly improved figurative language, verbal fluency, and dis-
course production abilities. However, the domain-specific intervention affected
the figurative language and discourse production abilities in AD.
In summary, deficits in WM should be noted because (1) they constitute the
most sensitive mechanism for neurological changes, including aging; (2) they
are a major initial indicator of AD; (3) they have a significant association with
MCI, a precursor symptom of AD; and (4) it is important to improve quality of
life in relation to various complex functions of everyday life, including communi-
cation. In particular, WM and language production are not only an extension of
language processing and interpreting but also serve as a practical indicator of
communication. Therefore, this study investigates the effects of WM intervention
on language production by patients with mild or moderate AD. The specific
research topics are as follows:
First, we aim to investigate the WM and language abilities of patients with mild or mod-
erate AD and normal controls in baseline, transfer-effect, and maintenance-effect
stages.

Second, we compare the differences in performance between groups and stages for
each task of WM and language production.

Third, the practical effects of WM intervention are presented for each task.

Materials and methods


Participants
This study was conducted on 39 AD patients, comprising 21 patients with mild
dementia and 18 patients with moderate dementia and 18 normal controls. Par-
ticipants were recruited in an elderly welfare centre, a day care centre, a care hos-
pital, and a centre for speech and language rehabilitation affiliated with a
university in Seoul.
AD was diagnosed according to the criteria of the National Institute of Neuro-
logical and Communicative Disorders and Stroke and Alzheimer’s Disease and
Related Disorders Association (NINCDS-ADRDA) (McKhann et al., 1984). In
addition, following the Clinical Dementia Rating (CDR) (Morris, 1993), the
patients were classified into mild (CDR=1) and moderate (CDR=2) groups. The
control group was determined to be normal in accordance with the Korean-
mini mental state examination (K-MMSE, Kang, 2006) and selected as the
control group that matched the distribution of the patients’ age, gender, and
education level. All participants had at least 6 years of education. The study
was conducted after receiving the approval of the institutional review board
of the relevant organization (#HUGSAUD461850).
6 M. S. LEE AND B. S. KIM

The results of the homogeneity test of age, gender, education, and K-MMSE
for the three groups displayed no significant differences in age (F = .528, p
= .593), gender (χ2 = .502, p = .778), and years of education (F = .108, p = .898).
The K-MMSE score was significantly different between the three groups (F =
67.658, p < .001).
The demographic and neuropsychological variables of the three groups,
such as age, gender, disease durations, years of education, CDR, and the
mean scores and standard deviations of K-MMSE, and the Informant-Report
Scale on Cognitive-Linguistic Abilities of the Elderly (ISCOLE) are presented
in Table 1.

Materials

Pre–post assessments
Pre–post evaluations were conducted before and after the interventions for two
sessions each. A word-span task and a digit-span task were performed to evalu-
ate WM ability before and after the interventions. The word-span task was com-
posed of forward and backward word span, and the stimuli of these tasks were
adapted from the words of Sung’s (2011) word-pointing task. The digit-span task
used forward and backward digit span, which are sub-tests of the Korean-Wechs-
ler Adults Intelligence Scale (K-WAIS) (Yeom et al., 1992). The number of words
and digits of the word and digit forward repetitions was 3–9, and the number
of those of the backward repetitions was 2–8.
In order to evaluate verbal-fluency ability, semantic and phonemic verbal-
fluency tasks were performed. In the semantic verbal-fluency task, the words
“animal” and “fruit” were spoken as much as possible for one minute (Kang
et al., 2000). Only the category “animacy” was used in this study, taking into
account the category attributes, in particular the differences in performance
according to the categories of animate and inanimate objects (Laws et al.,
2007). Phonemic verbal fluency was evaluated by tasks to use words beginning
with “ㄱ” and “ㄴ” for one minute. The phonemes were selected on the basis of

Table 1. Comparison between demographic and baseline neuropsychological variables in three


groups.
Central Mild AD (n = 21) Moderate AD (n = 18) Control (n = 18)
Age (yr.) 75.43 (4.33) 76.89 (5.85) 76.94 (5.67)
Gender (M:F) 10:11 7:11 9:9
Disease duration (months) 21.10 (6.30) 23.50 (4.82) -
Education level (yr.) 9.76 (2.61) 10.11 (2.83) 10.11 (2.78)
Education range 6–14 6–16 6–16
CDR 1 2 –
K-MMSE 18.90 (3.62) 13.50 (3.65) 25.33 (0.97)
ISCOLE 31.28 (8.72) 44.67 (19.27) 4.19 (2.11)
Scores in age, education level, and K-MMSE: mean(SD), Scores in gender: n, CDR: Clinical Dementia Rating, K-MMSE:
Korean-mini mental state examination, ISCOLE: Informant-Report Scale on Cognitive-Linguistic Abilities of the
Elderly (Lee, 2016).
NEUROPSYCHOLOGICAL REHABILITATION 7

Table 2. Pre-post assessments.


Total
Central Task score Task
Working memory Word span 0∼17 Forward
Backward
Digit span 0∼17 Forward
Backward
Language Word fluency – Semantic word fluency(animal/fruit)
production
Phonemic word fluency(ㄱ/ㄴ)
Confrontation 0∼15 K-BNT-15
naming
Word definition 0∼8 Noun definition test(cow/watermelon/chopsticks/
train)
Picture description 0∼15 PK-WAB-R(beach)
K-BNT-15: Short Form of the Korean Version-the Boston Naming Test, PK-WAB-R: Paradise Korea-Western Aphasia
Battery Revised, Total score: minimum ∼ maximum.

the frequency of phonemes in the spoken words of Korean adults and entries in
the Korean dictionary (Kang et al., 2000; Shin, 2008, 2010).
Confrontation-naming ability was assessed by the Short Form of the Korean
Version-the Boston Naming Test (K-BNT-15) (Kim & Kim, 2013). This is a task invol-
ving naming stimuli consisting of 15 nouns drawn in black and white lines.
The word-definition task involves describing in detail what each word means
after being presented with four nouns (“cow,” “watermelon,” “chopstick,” “train”).
The words were selected considering the semantic categories, which are animate
and inanimate categories, used in the Florida Semantic Battery (Raymer et al.,
1990). In addition, the words were selected on the basis of the relatively well-pre-
served functional and perceptual definition types despite the neurological
changes (Hodges et al., 1996).
The picture-description task utilized the subtest of “spontaneous speech” of
the “Beach” picture included in the Paradise Korea-Western Aphasia Battery
Revised (PK-WAB-R) (Kim & Na, 2012). When a picture stimulus drawn in black
and white lines is presented, the subject is asked to describe the contents in
the picture as much as possible. The evaluation items used in the pre–post
assessment are shown in Table 2.

Intervention
In order to train WM, a 3-step intervention protocol composed of WM mechan-
isms was applied. This is based on Zimmermann et al.’s (2014) WM intervention
programme and reconstructed according to the purpose of this study and
difficulty levels. Each step involved 12 types of task associated with the visuos-
patial sketchpad/phonological loop and episodic buffer/central executive func-
tioning (Table 3).
In the first step, sequencing figures, speaking lists of numbers, finding missing
pictures, and retelling a story immediately after reading it were performed. In the
second step, remembering position sequences, speaking lists of words, self-
8 M. S. LEE AND B. S. KIM

Table 3. Description of tasks on the working memory intervention protocol.


Central Step Task Description
Visuospatial sketchpad/ 1 Figures Remember the presented shapes and recall them in
Phonological loop sequence order
Number list Recall the list of numbers presented
2 Position Remember and say the location of the presented
sequence picture
Word list Say the list of words presented
3 Complex figures Remember and draw the pictures within a limited
time
Word generation Say/write the words of specific categories
Episodic buffer/ Central 1 Missing one Study the first picture and identify the missing one in
executive the second picture
Reading/ Read a story and retell it immediately
Retelling
2 Self-ordered task Point to a previously unselected picture from a set of
cards that are out of sequence
Reading/ Read a story and retell it again after 5 min
Retelling
3 Images and text See related pictures, read a part of a text, and
complete the text
Reading/ Read a story and answer questions
Recognition

ordering pictures, and retelling a story 5 min after reading it were used. The third
step consisted of remembering and drawing complex pictures, generating
words, seeing pictures and completing a text, and answering questions after
reading a story.

Procedures

This study was conducted in four stages. The flowchart is as follows: 2 sessions
for the baseline stage, 18 sessions for the intervention stage, 2 sessions for the
transfer-effect stage, and 2 sessions for the maintenance-effect stage, performed
three months after the end of the intervention phase (Figure 1).

Baseline stage
WM and language abilities were evaluated in two sessions before the interven-
tion in order to assess performance before applying the WM intervention proto-
col. Four tasks related to WM and five tasks related to language production were
randomly performed. The assessment time was 30–40 min on average per
session.
WM ability is determined by summing up the two subtasks that correspond
to the word-span and digit-span tasks. Verbal fluency was calculated as the
average score from the scores of each semantic verbal-fluency and phonemic
verbal-fluency task. For language abilities, confrontation naming was calculated
as the number of correct answers from the 15 items within 30 s, and word
definition was calculated as the average score of the four items, which were
rated as 2 (when the definition had two core meanings or more), 1 (when
the definition had one core meaning or two supplementary meanings or
NEUROPSYCHOLOGICAL REHABILITATION 9

Figure 1. Flow chart of working memory intervention protocol.

more), or 0 (when the definition was incorrect or for other responses). For the
picture-description task, the total score was determined by adding the infor-
mation (5 points) and fluency (10 points) according to the manual of PK-
WAB-R (Kim & Na, 2012).

Intervention stage
In the intervention stage, a WM intervention protocol was applied to the two
patient groups (Table 3). The intervention was carried out according to the pro-
tocol steps over a total of 18 sessions averaging 2–3 times a week for 30–40 min
per session.
Step 1. The first step of the visuospatial sketchpad and phonological loop
were composed of a “figure sequence” task in which participant was asked to
memorize the presented figures (e.g., a triangle and a rectangle) and then
recall them in order, and a “number list” task in which the participant is asked
to recount a list of numbers (e.g., 1-3-6). Between two and six figures or
numbers were included in the lists.
The episodic buffer and central executive stages feature a “missing item” task,
which involves identifying the item missing on a second card (e.g., dog-spoon-
socks) after having been shown a first card (e.g., dog-spoon-socks-bicycle), and
a “reading/retelling” task in which the participant is asked to read a story (e.g.,
10 M. S. LEE AND B. S. KIM

a story about a zoo) and retell the story immediately. Between two and six items
were included on the cards, and 10 different types of story were presented.
If the responses from all the tasks in the first stage were 70% or more, or if
the responses were 80% or more after the provisions of cues, the second stage
was carried out. The cues included repetition of visual or auditory stimuli,
semantic or phonemic cues of targeted words, and additional information
related to the story (e.g., there was another animal in front of the cages of
monkeys).
Step 2. The visuospatial sketchpad and phonological loop of the second stage
involved the “position sequence” task, in which the participant recalls and
describes the position of a presented picture (e.g., a block picture of another
shape) and the “word list” task in which the participant recalls a list of words pre-
sented to them (e.g., pencil -radish-fan). Between two and six pictures and the
words were presented in the lists.
The episodic buffer and central executive stage includes the “self-ordered”
task, in which the participant is asked to identify a previously unselected
picture from a set of cards that are out of sequence (e.g., ball-flower-pencil),
and the “reading/retelling” task, in which the participant reads a story (e.g., a
shopping story) and is asked to recount it 5 min later. The texts of the stories
had two to three sentences more than those in the first stage. Three to six pic-
tures were presented on the “self-ordered” task cards and 10 different stories
were presented in the “reading/retelling” task.
If more than 70% of the responses to all the tasks in the second stage were
correct, or if more than 80% of the responses were correct with the cues, the
third stage was presented. The cues included repetition of visual or auditory
stimuli, the drawing of selected pictures or writing in words (self-ordered task),
and additional information related to the stories (e.g., there is one vegetable
after buying a fruit).
Step 3. The visuospatial sketchpad and phonological loop of the third stage
are classified into the “complex figures” task of remembering a picture (e.g., a
geometric picture composed of lines and faces of different shapes) and
drawing it within a limited time, and the “word generation” task of saying and
writing words corresponding to a specific category (e.g., furniture). The pictures
were presented according to five difficulty levels. The categories of the “word
generation” task were based on the vocabulary used frequently by Korean
adults over 55 years of age (Kim et al., 2015), and a total of 10 categories were
selected, considering semantic typicality and word frequencies.
The episodic buffer and central executive stage involved the “images and
text” task of identifying a picture related to a text (e.g., a fruit store), reading a
piece of text, and completing the contents of the text, and the “reading/recog-
nition” task of reading a story (e.g., a story about maple leaves) and answering
related questions. Ten different texts and stories were presented and 3–5 ques-
tions were asked for each “reading/recognition” task.
NEUROPSYCHOLOGICAL REHABILITATION 11

Step 3 was performed until the end of the assignment, regardless of the per-
formance of the tasks. Cues included repetition of visual or auditory stimuli,
semantic cues (word generation task), and additional information related to
the stories (e.g., I went to the mountain in Gangwondo).

Transfer-effect stage
Post-evaluation was implemented for two sessions immediately after the inter-
vention was completed to analyze the effects of WM intervention on the two
groups. As with the baseline, nine tasks were used to assess WM and language
abilities. The tasks were randomized and took an average of 30–40 min per
session. The grading method was applied in the same way as it was during
the baseline stage.

Maintenance-effect stage
The same evaluations as the baseline and transfer-effect stages were reexamined
to assess the maintenance effect at 3 months after the end of the WM interven-
tion. The scoring method was applied in the same way as it was at the baseline
and transfer-effect stages.

Statistical analysis
The statistical analysis programme SPSS 25.0 version (IBM Corp., Armonk, NY,
USA) was used for data analysis in this study. Differences in the distribution of
age, gender, and years of education among the groups were confirmed by a
one-way analysis of variance (ANOVA) and a chi-squared test. The performances
before and after intervention and those of the maintenance-effect stage were
presented through descriptive statistics. The performances of the three groups
evaluated before and after the intervention and the maintenance-effect stage
were compared with repeated measures ANOVA and post-hoc analysis. In
addition, the effect size was presented to determine the intervention and main-
tenance effects of the three groups.

Results
Performances at each stage

The performance of WM and language abilities in the baseline, transfer-effect,


and maintenance-effect stages are shown by group (Tables 4 and 5). In the
mild AD group, the mean scores of the two WM tasks were lowest at the baseline
and highest at the transfer-effect stage. The same patterns were shown in the
four tasks of language-production abilities. The overall performance of the mod-
erate AD group was lower than that of the mild AD group, and the performance
in WM and language production were highest in the transfer-effect stage, with
the maintenance-effect stage next and the baseline stage lowest. The
12 M. S. LEE AND B. S. KIM

Table 4. Descriptive data for 3 stages in mild AD group (n = 21).


Maintenance effect
Central Task Baseline stage Transfer effect stage stage
Working memory Word span 5.81 (0.93) 7.33 (1.24) 6.90 (1.26)
Digit span 5.48 (1.08) 6.71 (1.45) 6.14 (1.11)
Language Word fluency 9.62 (2.18) 11.24 (1.67) 10.52 (1.86)
production
Confrontation 9.33 (2.27) 11.62 (2.06) 11.43 (2.06)
naming
Word definition 5.67 (2.27) 6.90 (1.34) 6.57 (1.66)
Picture description 9.00 (1.45) 10.43 (1.43) 10.14 (1.28)
Scores: mean (SD).

performance of the control group was the highest among the three groups in all
areas and in the order of the transfer effect, maintenance-effect, and baseline
stage (Table 6).

Comparisons of performance according to group, stage, and task

Comparisons of the differences in performance between groups and stages for


each task of WM and language production are presented in Table 7. The word
span of the WM tasks showed a significant difference among the three groups
(F = 100.97, p < .001), and the performance was significantly different for all
the three stages (F = 84.43, p < .001). Per the post-hoc test results in the mild
AD group, there was a significant difference between the baseline and trans-
fer-effect stages (p < .001) and between the baseline and maintenance-effect
stages (p < .01); however, the performance was not different between the trans-
fer- and maintenance-effect stages (p = .699). The moderate AD group showed a
significant difference only between the baseline and transfer-effect stages (p
< .05). The control group had significant differences between the baseline and
transfer-effect stages and between the baseline and maintenance-effect stages
(p < .05).
The performance of the digit-span task revealed a significant difference
among the three groups (F = 92.92, p < .001) and three stages (F = 60.42, p

Table 5. Descriptive data for 3 stages in moderate AD group (n = 18).


Transfer
Baseline effect Maintenance
Central Task stage stage effect stage
Working Word span 1.67 (1.37) 2.72 (1.18) 2.22 (1.31)
memory
Digit span .94 (1.39) 1.94 (1.39) 1.67 (1.24)
Language Word fluency 3.42 (1.48) 4.36 (1.03) 4.06 (0.98)
production
Confrontation 3.00 (0.77) 4.11 (0.96) 3.83 (0.86)
naming
Word definition 2.78 (0.94) 3.89 (0.96) 3.50 (0.92)
Picture description 1.94 (1.11) 3.00 (0.91) 2.67 (0.97)
Scores: mean (SD)
NEUROPSYCHOLOGICAL REHABILITATION 13

Table 6. Descriptive data for 3 stages in control group (n = 18).


Maintenance effect
Central Task Baseline stage Transfer effect stage stage
Working memory Word span 6.22 (1.11) 7.72 (1.49) 7.61 (1.42)
Digit span 5.89 (1.32) 7.28 (1.64) 6.67 (1.37)
Language Word fluency 10.50 (2.28) 12.28 (1.90) 11.78 (2.16)
production
Confrontation 10.94 (2.41) 13.06 (1.86) 12.17 (1.76)
naming
Word definition 6.44 (1.69) 7.17 (1.04) 7.00 (1.28)
Picture description 11.44 (2.48) 12.67 (2.50) 12.22 (2.26)
Scores: mean(SD).

< .001). There was a significant difference between the baseline and transfer-
effect stages in the mild AD group (p < .01); however, there was no difference
between the baseline and maintenance-effect stages (p = .249) or between the
transfer- and maintenance-effect stages (p = .408). In the moderate AD group,
only the difference between the baseline and the transfer-effect stage was sig-
nificant (p < .05). The control group had a significant difference between the
two stages (p < .001).
The verbal fluency of the language tasks was significantly different among the
three groups (F = 106.84, p < .001) and the three stages (F = 60.70, p < .001).
There was a significant difference between the baseline and transfer-effect
stages in the mild and moderate AD groups and the control group (p < .05).
The difference of performance in the confrontation-naming task was signifi-
cant among the three groups (F = 148.31, p < .001) and three stages (F = 50.34,
p < .001). In the mild AD group, the performance between the baseline and trans-
fer-effect stages and between the baseline and maintenance-effect stages was
significantly different (p < .01; p < .01), while there was little difference
between the transfer- and maintenance-effect stages (p = 1.00). In the moderate
AD group, there was also a significant difference between the baseline and trans-
fer-effect stages (p < .001) and between the baseline and maintenance-effect
stages (p < .01). The control group had significant differences between the

Table 7. Comparison of measures by group, stage and task.


Central Factor F df MSE p
Word span Group 100.97 2 4.10 <.001
Stage 84.43 2 0.34 <.001
Digit span Group 92.92 2 4.66 <.001
Stage 60.42 2 0.347 <.001
Word fluency Group 106.84 2 8.64 <.001
Stage 60.70 2 0.504 <.001
Confrontation naming Group 148.31 2 7.60 <.001
Stage 50.34 2 1.03 <.001
Word definition Group 35.40 2 5.50 <.001
Stage 46.14 2 0.34 <.001
Picture description Group 174.76 2 7.81 <.001
Stage 58.44 2 0.39 <.001
MSE: mean square error.
14 M. S. LEE AND B. S. KIM

baseline and transfer-effect stages (p < .01) and between the baseline and main-
tenance-effect stages (p < .05).
The performance of the word-definition task was significantly different among
the three groups (F = 35.40, p < .001) and the three stages (F = 46.14, p < .001). In
the mild AD group, there was no significant difference between the baseline and
maintenance-effect stages (p = .108) or between the transfer- and maintenance-
effect stages (p = .550), but there was for the baseline and transfer-effect stages
(p < .05). The moderate AD group showed a significant difference between the
baseline and transfer-effect stages (p < .01) and the baseline and maintenance-
effect stages (p < .05), but not for the transfer- and maintenance-effect stages
(p = .222). The control group had a significant difference only between the base-
line and the transfer-effect stages (p < .001).
The difference among the three groups and the three stages was also signifi-
cant in the picture-description task (F = 174.76, p < .001; F = 58.44, p < .001). In
the mild AD group, there was a significant difference between the baseline
and transfer-effect stages (p < .01) and between the baseline and mainten-
ance-effect stages (p < .05); however, the difference between the transfer- and
maintenance-effect stages was not significant (p = 1.00). Similarly, the moderate
AD group showed significant differences between the baseline and transfer-
effect stages (p < .01) and between the baseline and the maintenance-effect
stages (p < .05). The control group had a significant difference between the
two stages (p < .001).

Effect of the intervention


In order to compare the actual effect of the WM intervention, we analyzed the
effect sizes for each task (Figure 2). The task that exhibited the highest interven-
tion effect was the word span of WM (ηp² = .610) among other tasks. The inter-
vention effects were high in the order of the digit span of WM (ηp² = .528),
verbal fluency (ηp² = .528), and the picture description (ηp² = .520). The effective-
ness of the confrontation naming (ηp² = .482) and the word definition (ηp² = .461)
for language production was relatively low.

Discussion
The effect of WM intervention on language production by patients with mild or
moderate AD was investigated in this study. To this end, an intervention protocol
was applied consisting of tasks corresponding to the constituent areas of WM,
such as visual sketchpad/phonological loop and episodic buffer/central execu-
tive functioning, with performances at the baseline, transfer-, and mainten-
ance-effect stages being compared.
WM is a cognitive system for temporal access to representations required for
complex cognitive processing and is highly correlated with various cognitive-
NEUROPSYCHOLOGICAL REHABILITATION 15

Figure 2. Effect sizes presenting intervention effects by task. Effect size is a measure of partial
eta-squared (ηp²).

linguistic abilities, with different capacities depending on individuals (Barrett


et al., 2004; von Bastian & Oberauer, 2014). In other words, WM is the most
useful indicator of cognitive-linguistic competence (Oberauer et al., 2008), with
a negative impact on cognition and communication when it is impaired
(Alloway, 2009; von Bastian & Oberauer, 2014). Thus, WM interventions are
useful not only for WM capacity but also for enhancing related cognitive-linguis-
tic abilities and overcoming cognitive-communicative deficiencies due to aging
or neurological disorders (Klingberg, 2010; Morrison & Chein, 2011).
The results of examining the WM and language-production abilities of each
stage in this study showed that all performances of the mild and moderate
AD groups were lowest in the baseline stage and highest in the transfer-effect
stage. In other words, a transfer effect of WM intervention on WM and
language-production capability occurred. This is due to the expansion of WM
capacity, which also improves the performance of non-trained tasks that share
the changes of the trained tasks (Klingberg, 2010). The performance of the
word-span and digit-span tasks that were not trained was improved; there
may have been a “near transfer” effect through the intervention. In addition,
the improved performance in the language-production tasks reflects the “far
transfer” effect, which implies the transfer from WM capacity to cognitive-linguis-
tic task abilities.
In general, the effects of WM intervention appear in two ways: WM capacity
and efficiency (von Bastian & Oberauer, 2014). If WM capacity increases
through intervention, the brain area that limits WM capacity changes because
more items can be simultaneously held than before the intervention. In other
16 M. S. LEE AND B. S. KIM

words, the functional brain network associated with WM changes due to the
intervention (Langer et al., 2013). Enhanced WM capacity also improves cogni-
tive-linguistic ability’s capacity to use the same structural resources as those
relied on by WM through redundant activation. This is also confirmed through
the neurological overlap of neurons (Dahlin et al., 2008).
Further effectiveness of the intervention is shown by the capacity to learn
knowledge and skills, such as the use of strategies, chunk learning, automatiza-
tion of basic processing, and allocations of attention, which make it possible to
use WM capacity more efficiently (von Bastian & Oberauer, 2014). Unlike capacity
expansion, enhancement of efficiency varies depending on the data or processes
utilized. For example, strategies for a particular paradigm, such as n-back or
complex span tasks, can be learned (Dunlosky & Kane, 2007). However, even if
the learned strategy is effective, the transfer to a task with a new structure or
data is limited (Lustig et al., 2009).
In this study, we show how WM intervention affects each task of language
production. The performance of verbal fluency was significantly different
between the baseline and transfer-effect stages in both mild and moderate
AD groups. Many studies of elderly adults have reported the transfer effect of
WM intervention on verbal fluency. The results of a home-based verbal WM inter-
vention for 41 elderly people showed great progress in performance of verbal-
fluency tasks, as well as processing of sentential memory and syntactic ambiguity
(Payne & Stine-Morrow, 2017). The eight-week intervention, consisting of WM
and higher-level cognition, demonstrated the far transfer effect on verbal-
fluency capabilities, with a near transfer effect of WM (Goghari & Lawlor-
Savage, 2017).
The degradation of verbal fluency due to aging and neurological disorders
results from deficits in overall information processing, not the loss of knowledge
of language itself (de Paula & Malloy-Diniz, 2013; Lee & Kim, 2018, 2019). If infor-
mation processing is not smooth, short-term memory and WM deteriorate,
which ultimately leads to difficulty in verbal fluency. This decreases the
number of words produced in verbal-fluency tasks and a deterioration in the
response strategy for semantic typicality and efficient association (Unsworth
et al., 2012). The transfer effect in this study, regardless of the severity of AD,
is based on this correlation between WM and verbal fluency.
The confrontation-naming abilities in this study were significantly different
between the baseline and transfer-effect stages and between the baseline and
maintenance-effect stages for all the three groups. Neurological changes, such
as aging and AD, impair confrontation-naming abilities by restrictions in WM
and executive functions, distraction of attention, and a heavy reliance on
already learned stereotypes, empirical knowledge, and schematics (Peach &
Shapiro, 2012). Thus, by facilitating the use and learning of strategies through
various verbal and non-verbal WM interventions, WM capacity can be used
efficiently (von Bastian & Oberauer, 2014), which can improve confrontation-
NEUROPSYCHOLOGICAL REHABILITATION 17

naming abilities. In particular, both the transfer and maintenance effects of the
performance of the confrontation-naming task were able to substantiate this
mechanism.
The word-definition task, which reflects language-production ability based on
the semantic processing, requires knowledge of target words and metalinguistic
ability for defining words. Thus, the performance of word definition can be an
indicator of the deterioration of complex cognitive-linguistic abilities due to
neurological changes (Hough, 2007). In particular, a word-definition task is
more sensitive than a confrontation-naming task is in that AD patients tend to
generate fewer types, incorrect information, and fewer core meanings while per-
forming word-definition tasks than healthy adults do (Marinellie & Johnson,
2004). Thus, the effect of cognitive interventions, including WM can be promi-
nent in the performance of this task. Through WM intervention, it is possible
to reduce inappropriate vocabulary and greatly improve the efficiency of infor-
mation transmission while performing the task. In the present study, the per-
formance of the word-definition task was significantly different between the
baseline and transfer-effect stages in the mild AD group. The performances
were also significantly different between the baseline and transfer-effect
stages and between the baseline and maintenance-effect stages in the moderate
AD group. It is noteworthy that the maintenance effect of the moderate AD
group proves the clinical utilization of WM intervention.
In the picture-description task, both AD groups showed the transfer and main-
tenance effects. When compared to the other tasks, the performance of the
picture-description task showed a relatively large effect size. The tasks of dis-
course production sensitively reflect neurological changes because semantic,
syntactic, and phonological abilities need to be integrated to generate discourse
(Burke & Shafto, 2007; Kim & Lee, 2019b). In particular, attention, executive func-
tion, and WM are directly related to the various abilities in discourse production,
such as phonological knowledge, semantic efficiency, syntactic ability, refine-
ment of macrostructure, cohesion, coherence, and appropriateness of infor-
mation (Fleming & Harris, 2008; Kim & Lee, 2019b; March et al., 2009). The WM
intervention in this study consisted of subtasks associated with visual sketch-
pad/phonological loop and episodic buffer/central executive function based
on Baddeley’s (2000) WM model. Thus, our WM intervention dealt with attention
control, manipulation and storage of information from other subsystems and
verbal information, divided attention, decoding of visuoperceptual/motosensory
and image code, and the interaction of WM subsystems and other cognitive
systems. The highest effect size of the picture-description task resulted especially
from the fact that high-level language functions, such as discourse production,
can be maximized through complex WM interventions and related stimulations
(Zimmermann et al., 2014).
As a result of this study, the transfer effect was shown for all tasks in the two
groups. In particular, the far transfer effect was noteworthy in that the effect was
18 M. S. LEE AND B. S. KIM

related to language-production tasks associated with the WM mechanism. Con-


sidering that the knowledge and skills acquired directly through intervention are
limited, the far effect is a desirable indicator of intervention in terms of efficiency
and WM capacity (von Bastian & Oberauer, 2014).
The intervention-specific aspects are the factor that influences our interven-
tion effect. This includes the attributes of the tasks, the adjustment of task
difficulties, and the intensity and duration of the interventions. The intervention
protocol applied to this study consisted of tasks based on a multi-paradigm of
WM, which can be clinically useful because it utilizes diversified tasks relative
to a single paradigm (Brehmer et al., 2012; Shiran & Breznitz, 2011). The diversity
of tasks increases the motivation of the participants, and the unadjusted cogni-
tive-linguistic processes are applied in different contexts to promote a real trans-
fer effect. The difficulty of the tasks also affects the intervention effect. In this
study, adaptive training algorithms were used that phased in the difficulty
level of the tasks stepwise. These algorithms were based on the hypothesis
that plasticity is promoted when there is a “prolonged mismatch” between orga-
nismal functionality and environmental needs (Lövden et al., 2010).
There are diverse views on the effects of the intensity and duration of WM
interventions. The number of intervention sessions per research varies from 3
to 100 sessions (Borella et al., 2010; Schmiedek et al., 2010), and the duration
of one session varies from 10 min to 30–45 min (Owen et al., 2010; von
Bastian & Oberauer, 2013). Although there is no agreement on the optimal inten-
sity and duration for the effects of WM intervention, it is reported that sporadic or
spaced training is more effective than intensive training when intervening in
fluid areas, as in the case of WM, compared to crystalline areas (Penner et al.,
2012). Therefore, in this study, we designed the intervention protocol to maxi-
mize the intervention effectiveness in light of the intervention intensity and dur-
ation in previous studies that proved the effect of WM intervention and the fact
that WM involves a fluid area.
Another factor influencing the intervention effect of this study is the paradigm
of intervention of WM. In this study, a CT paradigm comprising tasks related to
the subsystems of the WM mechanism, such as visuospatial sketchpad, phono-
logical loop, episodic buffer, and central execution, was applied. This was advan-
tageous for maintaining attention even when facing internal and external
disturbances and enhancing fast encoding and retrieval. In addition, intervention
difficulties can be adjusted according to the various levels of cognitive abilities of
the participants (Lee & Kim, 2020). Indeed, several studies have proven the effec-
tiveness of the CT paradigm on language production. Zimmermann et al. (2014)
explained that high-level language function is maximized through complex WM
intervention and stimulation. In the study of AD (Lee & Kim, 2020), regardless of
the severity, the intervention effect on the ability to produce a discourse was sig-
nificant. That is, discourse production is sensitive to changes in WM capacity
because it requires integrated language abilities comprising semantic
NEUROPSYCHOLOGICAL REHABILITATION 19

knowledge, syntax, and pragmatic skills (Kim & Lee, 2019a). In other words, pho-
nological knowledge, semantic efficiency, syntactic utilization, elaboration of
macrostructure, cohesion, coherence, and informativeness that are necessary
for discourse tasks are directly related to changes in WM (Kim & Lee, 2019a).
The WM intervention used in this study has high cognitive loads, requires
highly intensive cognitive tasks, and includes sequential processing and frequent
memory updates (Chein & Morrison, 2010). Further, it focuses on limiting the use
of domain-specific strategies, minimizing automatization, and exploiting chal-
lenges and stimuli across several modalities (Morrison & Chein, 2011). Training
different types of tasks not only strengthens motivation but also facilitates
actual transfer when targeted cognitive processing is practiced in different con-
texts. Therefore, it is known that the transfer effect is greater than that of non-
sequential, non-adaptive, and single-modality training (Olson & Jiang, 2004).
Various categories of cognitive-language abilities that depend on WM capacity
are improved, and thus, it works positively on the functions of everyday life,
especially because they have a high correlation with cognitive control, fluid intel-
ligence, and reading comprehension (Morrison & Chein, 2011). Most of all, the
WM intervention used in this study contributes greatly to the transfer to
language production ability based on high-level and complex processing (Lee
& Kim, 2019; Peach & Shapiro, 2012).
In terms of the maintenance effects, the intervention of this study proved
effectiveness only for some tasks. Among the WM tasks, the result of the
word-span task showed a maintenance effect in the mild AD group. In the
language-production tasks, performances in the confrontation-naming and
picture-description tasks showed the maintenance effects in both groups, and
that of the word-definition task showed a maintenance effect only in the mod-
erate AD group. The maintenance effect of WM intervention varies from study to
study because the complexity of the task and the coordination of procedures
affect the performances of participants (Buschkuehl et al., 2008; Li et al., 2008).
There is a report that the effect is maintained until 3 or 8 months after the com-
pletion of the intervention (Borella et al., 2010; Li et al., 2008), but there is also
another report that the performance will inevitably decrease after the interven-
tion (Buschkuehl et al., 2008). The limited maintenance effects of this study
coincide with these variations.
In summary, this study demonstrated that WM intervention for AD patients is
effective in language production. In addition, it provided an opportunity to
improve clinical utilization by showing how the transfer and maintenance
effects for each task of language production vary with evidence-based practices.
The protocol of this study can be used as an important basis for further interven-
tion to improve the language abilities of AD patients.
Nevertheless, this study has some limitations. First, the multiple-paradigm
intervention used in the study has the disadvantage that it cannot clearly identify
the influencing factors of the effects, in contrast to a single-paradigm or multi-
20 M. S. LEE AND B. S. KIM

factorial approach. In other words, it is unclear which paradigm in the same


mechanism promoted WM capacity, unlike a multi-factorial approach aimed at
various cognitive-linguistic areas and a single-paradigm approach consisting of
tasks that apply one paradigm. Further research warrants the development
and application of a diversified intervention protocol that considers these
aspects. Second, the maintenance effects of this study were limited by tasks or
groups when compared with the transfer effects. One of the influencing
factors of this result is individual differences. In particular, the initial cognitive-lin-
guistic abilities, genetic predisposition, motivation, and personalities of the
target group may have had some effects on the intervention. In addition, the
characteristics, procedures, and implementation methods of the tasks may be
variables that affect the maintenance effects. In the future, it will be necessary
to consider the influencing factors on the maintenance effect in various ways
and to design a method to maintain the effectiveness of the intervention. Fur-
thermore, investigations of the maintenance effect after an additional 3
months will be needed to determine the changes in cognitive-linguistic abilities
after the intervention.

Acknowledgments
The authors thank to the participants.

Disclosure statement
No potential conflict of interest was reported by the author(s).

ORCID
Bo Seon Kim http://orcid.org/0000-0002-8351-1417

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