Reminder of important clinical lesson

CASE REPORT

Difficulty with learning of exercise instructions
associated with ‘working memory’ dysfunction
and frontal glucose hypometabolism in a patient
with very mild subcortical vascular dementia
with knee osteoarthritis
Kenji Takeda, Kenichi Meguro, Naofumi Tanaka, Masahiro Nakatsuka
Department of Geriatric
Behavioral Neurology, Tohoku
University Graduate School of
Medicine, Sendai, Miyagi,
Japan
Correspondence to
Professor Kenichi Meguro,
k-meg@umin.ac.jp

SUMMARY
We present a patient with no dementia, depression or
apathy, who had difficulty in learning self-exercise
instructions. The patient was an 80-year-old righthanded woman who was admitted to a rehabilitation
unit to receive postoperative rehabilitation after a femoral
neck fracture. She was instructed quadriceps isometric
exercises to perform 10 repetitions and to hold each
stretch for 10 s. She performed the exercise correctly
with motivation, but she had difficulty in learning the
number of repetitions and the duration of each
stretch. She had no history of cerebrovascular accident
and the neurological examination was normal.
Neuropsychological testing, MRI and 18F-fluoroD-glucose-positron emission tomography (FDG-PET) were
performed to examine the neural mechanisms associated
with this difficulty in learning instructions.
Neuropsychological tests revealed dysfunction of working
memory while other cognitive domains were relatively
preserved. Her neuropsychological tests scores were
(1) Mini-Mental State Examination: 24 (mild cognitive
impairment), (2) Geriatric Depression Scale-15: 2 (no
depression), (3) Apathy Scale: 2 (no apathy), (4) digit
span forward: 5 (normal), (5) digit span backward:
2 (impaired), (6) visuospatial span forward: 4 (normal),
(7) visuospatial span backward: 2 (impaired), (8) frontal
assessment battery: 11 (normal), (9) Weigl test:
0 (impaired), (10) trail making test A: 52 s (normal),
(11) train making test B: failed (impaired). T2-weighted
and fluid-attenuated inversion recovery MRI showed high
signal-intensity lesions in the cerebral deep white matter.
FDG-PET revealed hypometabolic areas in the bilateral
frontal lobes, particularly in the bilateral dorsolateral
frontal area, anterior cingulate cortex and orbitofrontal
cortex. One of the possible neural mechanisms
underlying the learning difficulties in this patient may
have been partial blockage of the cingulofrontal network
by deep white matter lesions.

BACKGROUND
To cite: Takeda K,
Meguro K, Tanaka N, et al.
BMJ Case Rep Published
online: [ please include Day
Month Year] doi:10.1136/
bcr-2013-008577

Motor learning is a key to a successful outcome of
physical therapy. If a patient acquires declarative
memory of instructions on procedures for motor
learning, efficient physical therapy can be performed.
A patient who understands and remembers the contents of home exercise instructions given by a therapist and correctly exercises is likely to maintain or

Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

improve physical functions. For instance, a home
exercise programme, including muscle strengthening,
muscle stretching and active range of motion exercises, is effective for improving function and decreasing stiffness and pain in patients with osteoarthritis
of the knee.1
With ageing of the population, many elderly
patients require physical therapy. Bone and joint
diseases are the commonest diseases causing subsequent dependence in activities of daily living, and
rehabilitation therapy plays an important role in
treatment.2
Neuropsychological inhibitors of physical therapy
include dementia,3 depression4 and apathy.5 In addition to general cognitive impairment, explicit motor
learning may inhibit physical therapy, linked to
various domains, including memory, executive function, etc. However, it is unknown which domain is
impaired in patients with disability of learning explicit instructions.
We experienced a patient transferred to our hospital for rehabilitation after surgery for trochanteric
fracture complicated with knee osteoarthritis. She
was given instructions on isometric contraction
exercise of the quadriceps for improvement of gait
performance, but she did not remember these
instructions, although she did not have dementia,
depression or apathy. Therefore, we studied the
neuropsychological characteristics and neurological
background, using neuropsychological tests, head
MRI and 18f-fluoro-D-glucose-positron emission
tomography (FDG-PET).

CASE PRESENTATION
The patient was an 80-year-old right-handed
woman with 8 years of education. She had suffered
a left femoral neck fracture and had left knee osteoarthritis. She lived with her husband, who had suffered a stroke, and took care of him and did their
housework independently. She had a mild and
nervous personality. She had a history of hypertension that had been well controlled by medication
for 10 years, but no history of cerebrovascular accident. She had suffered pain in her left knee due to
osteoarthritis for 5 years.
Four weeks earlier, she had fallen and sustained a
fracture of the left femoral neck. She was admitted
to the emergency department in the hospital and
1

Reminder of important clinical lesson
was treated with osteosynthesis on that day. Her ability to walk
gradually improved as her left hip pain improved, and she progressed to walking with a cane at 4 weeks postoperatively.
However, her gait was still imbalanced due to postoperative disability and left knee pain, which deteriorated after the operation. Therefore, she transferred to our hospital for further
improvement.
A general physical examination revealed no abnormal findings. Her blood pressure was controlled. There were no abnormal findings in neurological examinations and her consciousness
was alert. Regarding verbal memory, the patient remembered
the episode of the fall and the names of people who she met on
a daily basis. In visual memory, she remembered the faces of
people who she met on a daily basis, and the locations of the
toilet and her bedroom in the rehabilitation ward. She was
oriented to time and place, and she had no apraxia and no
impairments in language, attention, visuospatial function and
executive function. Her behaviour caused no difficulties in her
daily life, and she was polite, amiable and motivated in her
rehabilitation.
Based on the Diagnostic and Statistical Manual of Mental
Disorders-IV criteria, a board-certified neurologist (KM) and a
geriatrician (Hiroshi Ishii examined her and found no apparent
dementia or depression or apathy. However, taking her MRI
findings into consideration, she met the criteria for very mild
stage of subcortical vascular dementia.6 Her Mini-Mental State
Examination (MMSE) score was 24. Screening for depression
was performed using the 15-item Geriatric Depression Scale,7
on which a value ≥5 indicates clinically depressive. She obtained
a score of 2. Apathy was evaluated on the Apathy Scale consisting of 14 items, on which a value ≥16 indicates clinical apathy.8
Her score was 2. Therefore, she had no apparent dementia,
depression or apathy. However, she had scores of 1 on subtests
of serial 7s.

INVESTIGATIONS
Instructions for quadriceps exercise
The patient was instructed to press the back of knee against a
rolled towel while trying not to lift her heel off the bed while in
the supine position,9 to hold the muscles tightly contracted for
a count of 10, then relax and to repeat this exercise 10 times.
Immediately after the first instruction, she was able to perform
precisely. She was then asked to learn the exercise instructions
to allow the exercise to be performed at home after discharge to
control knee pain.
In the next rehabilitation session, the patient was asked by the
therapist about the procedure of quadriceps isometric exercises

before the exercise was performed, with a question such as
‘Explain the exercise using the towel.’ She could demonstrate
the action of pushing down on the towel with her knee, but
gave the wrong numbers for the counts during pushing down
and for repetitions. Therefore, the therapist asked her to recall
the exercise instructions at the beginning of every session (at
least once a day) until she could remember the right numbers.
The exercise was performed at least once a day in the morning
or afternoon, and sometimes twice a day. The patient required
14 days before she was able to give the correct numbers in the
instructions.

Course of learning
To compare with this case, we recorded the learning process in
other patients without dementia as a control. Clinical data for
eight controls aged 79.5±8.6 years are shown in table 1.
They underwent surgery for disorders of bones or joints of
the lower extremities and were given the same instructions.
None of them showed marked impairment (mean
MMSE=25.0) nor met the criteria for depression or apathy.
Step-by-step progresses in motor learning are shown in figure 1.
The controls achieved memory of motor learning in 4.0
±1.2 days, whereas the patient needed 14 days to remember the
instructions. The patient walked by herself with a straight cane
because of a pain relief and was discharged 8 weeks after she
was transferred to the rehabilitation unit of our hospital.

Physical therapies that did and did not require time
for motor learning
The patient underwent other physiotherapy exercises. She was
instructed to remember the contents of three kinds of exercises:
‘exercise of legs on the bed’, ‘side walk between parallel bars’
and ‘stair-stepping exercise’.
The ‘exercise of legs on the bed’ consisted of lifting the legs
in the supine position, rotating the hip joint in the lateral position and extending the hip joint in the prone position, and was
performed to increase muscle strength. This exercise was
repeated 10 times to provide the patient with an appropriate
load in self-exercise. She was asked to remember the number of
repeats, and was able to recall this number and answer by rote
at the beginning of the next or subsequence sessions.
The ‘side walk between parallel bars’ involved sideways
walking holding parallel bars with both hands, with the goal of
improving the gluteus medius. To effectively train this muscle, it
is necessary to exercise while keeping the toes straight ahead at
a right angle to the parallel bars. Therefore, the patient was
asked to remember ‘to keep your toes straight ahead’. She was

Table 1 Background information for controls
Patient

Age (years)

Gender

Education (years)

MMSE

Diagnosis

GDS-15

Apathy Scale

A
B
C
D
E
F
G
H
Average (SD)

61
75
77
83
81
93
84
82
79.5 (8.6)

Female
Female
Female
Male
Female
Female
Female
Female
—

12
8
8
8
9
8
8
8
8.6 (1.3)

29
26
26
25
24
24
23
23
25 (1.9)

Left hip fracture after surgery
Right patellar fracture after surgery
Right tibial diaphyseal fracture after surgery
Right hip fracture after surgery
Right hip osteoarthritis after surgery
Right trochanteric fracture after surgery
Right trochanteric fracture after surgery
Left hip fracture after surgery
—

0
1
1
1
4
4
4
3
2.3 (1.6)

1
2
4
3
12
5
7
11
5.6 (3.8)

MMSE, Mini-Mental State Examination; GDS, Geriatric Depression Scale.

2

Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

Reminder of important clinical lesson
Figure 1 Course of learning of
isometric contraction exercise of the
quadriceps. Dashed lines indicate the
course of learning in cases A–H, all of
whom were postoperative patients
without dementia. The patient in this
study, whose course is indicated by the
blue solid line, took much longer to
learn instructions, compared with
patients who had good general
cognitive function.* Explanation
of figures on the vertical axis:
1: The patient understood the exercise
of pushing down on a towel. 2:
In addition to 1, the patient explained
the number of counts or sets. 3: In
addition to 1, the patient explained
the numbers of counts and sets.

able to remember this point and answer by rote at the beginning
of the next or subsequent sessions.
The ‘stair-stepping exercise’ required learning to put the legs
and a cane on steps. After surgery for hip fracture, it is safer to
step stairs with a cane to reduce the load on the operated leg.
Therefore, the procedures for stepping stairs were to place the
cane, the non-operated leg and the operated leg in order when
stepping up; but the cane, the operated leg and the nonoperated leg in order when stepping down. Consequently, the
non-operated leg always receives the greater load. The patient
was asked to remember the order of stepping stairs and after
learning this information she could explain the order for stepping up and down by rote at the beginning of the next or subsequent sessions.
Among all the physical therapies for which the patient was
asked to remember instructions, it took most time for her to
remember the counts when pushing on a towel at the popliteal
fossa and the number of repeats in isometric contraction exercise of the quadriceps.

Comparison of physical therapies that did and did not
require time for motor learning
The physical therapies that did and did not require time for
motor learning had two differences: the number of issues to
keep in mind and familiarity with the motion of the therapy.
For example, in ‘exercise of legs on the bed’, a physical therapy
that did not require time for motor learning, the patient was
required only to memorise the ‘number of exercises’ of lifting
the legs, rotating the hip joint and extending the hip joint
10 times each. Similarly, the side walk only required remembering ‘to keep the toes straight ahead’, and in the ‘stair-stepping
exercise’ the patient only had to remember to put the cane and
legs down in particular orders when stepping up or down. In
addition, these motions were relatively familiar to the patient.
Therefore, these were defined here as ‘single task’ exercises.
In contrast, in the isometric contraction exercise of the quadriceps, which did require time for motor learning, the patient
needed to remember both the counts when pushing on the
towel at the popliteal fossa and the number of repeated exercise
sets, that is, two tasks. Furthermore, the patient was unfamiliar
with the motion of pushing down on the towel at the popliteal
fossa. Therefore, this exercise was defined here as a ‘dual task’
exercise.
Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

The patient attained long-term memory in the single task, but
the dual task remained in the ‘short-term memory’ and required
much more time to reach the long-term memory (figure 2).
Neuropsychological test results and MRI and PET images of the
head and were analysed to examine why the patient took much
longer to remember the instructions for isometric contraction
exercise of the quadriceps, despite the absence of dementia,
depression and apathy.

Examination of frontal lobe function
The patient had poor scores for calculations and spelling words
backwards in the MMSE. Therefore, frontal lobe function was
examined.

Digit span
Performance on forward and backward digit span tests is associated with verbal ‘short-term memory’ and verbal ‘working
memory,’ respectively. In clinical settings, ‘short-term memory’
in this study was defined as the retention of information in a
very short time, whereas ‘working memory’ was considered to
be processing information retained as ‘short-term memory.’ The
mean forward and backward digit span values were 5.6±1.1
and 4.3±1.1, respectively, in patients aged 83±3.6 years.10
These were 5 and 2, respectively, in our patient.

Visuospatial span
Spatial forward and backward span tests were related to visuospatial short-term and ‘working memory,’ respectively. The
mean spatial forward and backward span values were 4.8±0.8

Figure 2 Differences in commitment to memory between single and
dual tasks. The patient attained long-term memory for a single task,
but dual tasks remained in the short-term memory. A much longer
period was required to attain long-term memory for the dual task.
3

Reminder of important clinical lesson
and 4.6±0.9, respectively, in patients aged 83±3.6 years.10 In
our patient, these were 4 and 2.

Frontal assessment battery
The mean total score is 13.8±2.6 in patients aged≥80 years.11
The score for our patient was 11 out of 18.

Weigl test
A subject classifies 12 blocks marked with a heart, club,
diamond or spade and with differences in size, colour, shape or
thickness, using five factors: mark, colour, shape, size and thickness of blocks. The score for each factor ranges from 0 to 3 and
the total possible score is 15.12 This task requires a patient to
keep new and previous information in mind, choose appropriate
objects or decisions, maintain the set (structure) and change
(shift) them in accordance with updated information. The mean
total score was 13.0±0.0 in patients aged 70–85 years.13 The
score for our patient was 0 out of 15.

Trail making test
A previous study showed that the mean times to complete tests
A and B were 73.9±26.0 and 229.1±94.9 s, respectively,
in patients aged 75–84 years.14 Our patient completed test A in
52 s, but failed to complete test B due to making many errors in
numbers and letters and being unable to revise these errors.

Imaging findings
The patient underwent head MRI and FDG-PET to examine
brain function. MRI (figure 3) revealed deep white matter
changes, but no cerebrovascular lesions were found.
Glucose metabolism in the brain was evaluated with
FDG-PET. Three-dimensional stereotactic surface projections
were generated using a Z score map (figure 4). The results
showed reduced metabolism in the bilateral frontal lobes, and
particularly in the dorsolateral prefrontal area, anterior cingulate
and orbital area.

OUTCOME AND FOLLOW-UP
The patient had reduced working memory, and consequently
she required a long time to remember instructions for isometric
contraction exercise of the quadriceps. The MRI revealed deep
white matter changes. The FDG-PET showed reduced metabolism in the bilateral frontal lobes, and particularly in the dorsolateral prefrontal area, anterior cingulate and orbital area. No
follow-up data were obtained.

DISCUSSION
The patient had reduced frontal lobe function, particularly for
‘working memory,’ and consequently she required a long time
to remember instructions for isometric contraction exercise of
the quadriceps, despite the absence of apparent dementia,
depression and apathy.

Limitations in neuropsychological and behavioural
assessments
The main question is the inability of the patient to learn 10
repetitions of quadriceps exercise with a 10 s hold. There is
enough evidence to prove that in the elderly with decreasing
working memory they are able to hold the instructions within
their small focus of attention.15 In prima facie it seems the
patient had other cognitive domains affected too, which barred
her from learning the exercise instructions. Hence the choice of
neuropsychological tests is critical. Also, the areas where the
lesions have been found play an important role in problem
solving, executive memory, abstract thinking, reward anticipation, decision-making, etc. Hence a comprehensive evaluation
through appropriate neuropsychological tests was important to
strongly correlate the lesion areas and its affection to patient’s
exercise performance. However, limited time in the rehabilitation ward where many patients should be treated at the same
time prevented us from performing such detailed neuropsychological tests. Despite the limitations, we consider that the case
could provide an evidence of rehabilitation for dementia.

Comparison with results of previous imaging studies
of brain functions
Using functional MRI, the left dorsolateral prefrontal area, the
temporal lobe and bilateral cingulate gyrus were found to be
activated in the trail making test-B16 and the bilateral inferior
frontal sulcus, supramarginal gyrus and anterior cingulate were
activated in the Wisconsin Card Sorting Test.17 Using PET, the
left supplementary motor area and the posterior parietal lobe
were found to be activated in verbal ‘working memory,’ while
the right supplementary motor area, posterior parietal lobe and
occipital lobe were activated in the visuospatial working
memory of Broca’s area.18 These areas and the area with
reduced glucose mechanism in the patient are shown in figure 5.
The patient had poor scores in the trail making test B, the
Weigl test, for counting forward and for visuospatial backward
span. The Weigl test and Wisconsin card sorting test19 are
sorting tests, and therefore the brain area activated in the
respective tasks is likely to be similar. As shown in figure 5, the

Figure 3 Head MRI. Fluid-attenuated
inversion recovery (left) and
T1-weighted (right) images revealed
deep white matter changes around the
cerebral ventricle, but no
cerebrovascular lesions were found.

4

Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

Reminder of important clinical lesson
Figure 4 Fluorodeoxyglucose
positron emission tomography images
with a standardised Z score map of
the whole brain glucose metabolism
was reduced in the bilateral frontal
lobes, particularly in the dorsolateral
prefrontal area, the anterior cingulate
and the orbital area. 3D-SSP,
three-dimensional stereotactic surface
projections; GLB,global; R.LAT,right
lateral; L.LAT,left lateral; R.MED,right
medial; L.MED,left medial.

areas with reduced mechanism were similar to the cerebral areas
found to be activated in neuropsychological tests, except for the
area in the right dorsolateral prefrontal area, which was not
explained by the neuropsychological tests.

Association with ‘working memory’
Recent studies suggested that the working memory is involved
in retaining new information as long-term memory.20 In daily
life events commonly occur for which information can be easily
recalled when we repeat to rehearse the information in our

mind. Studies of phonological working memory by Davachi
et al21 and of visuospatial working memory by Ranganath
et al20 suggested that maintenance of information in the
working memory involves use of long-term memory.
Kondo et al22 classified 20 healthy volunteers into largeworking and small-working memory groups: the patients were
asked to solve the calculation while keeping the target word in
mind (dual task), and then asked to recall the word. The
patients with large working memory recalled more words, and
functional MRI showed that the anterior cingulate was

Figure 5 Areas with reduced glucose
mechanism in the patient and cerebral
areas activated by neuropsychological
tests in previous studies. (1) Areas
activated in trail making test B to a
greater extent than in test A on
functional MRI,16 (2); Areas activated
in the Wisconsin Card Sorting Test on
functional MRI,17 (3); Areas activated
in the verbal working memory task on
positron emission tomography (PET),18
(4); Areas activated in the visuospatial
working memory task on
PET.18Activation in the right
dorsolateral prefrontal area (red circle)
could not be explained based on
previous results for activation in
neuropsychological tests. 3D-SSP,3D
stereotactic surface projections; GLB,
global; R.LAT, right lateral; L.LAT,left
lateral; R.MED,right medial; L.MED,
left medial.

Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

5

Reminder of important clinical lesson
activated. Furthermore, in patients with large working memory,
the cingulofrontal network was strongly associated with
working memory.
In our patient, FDG-PET showed reduced metabolism in the
anterior cingulate, and ‘working memory’ was also reduced.
Therefore, the patient may have received a greater load that
overwhelmed the reduced ‘working memory’ in the dual task of
isometric contraction exercise than in the single tasks. She completed the exercise under supervision of a therapist, suggesting
that her ‘working memory’ was sufficient to complete the task,
but not enough to transform the instructions into long-term
memory. This may explain the longer time required for motor
learning.

Competing interests None.
Patient consent Obtained.
Provenance and peer review Not commissioned; externally peer reviewed.

REFERENCES
1

2
3

Association with deep white matter changes
Head MRI detected no cerebral stroke, but showed white
matter changes around the cerebral ventricle. Swartz et al23
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white matter changes around the cerebral ventricle in our
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Application to rehabilitation therapy
As described above, a key to a successful outcome of rehabilitation therapy is for the patient to learn the exercise procedures.
In our case, the patient took longer to learn the exercises, but
reached the learning goal in a step-by-step manner. Therefore,
when instructing a patient with reduced ‘working memory’, it
might be effective to divide target tasks into simple step-by-step
instructions to decrease the amount of information given at one
time. In addition, a motion with which a patient is unfamiliar
might cause a greater load to be placed on the ‘working
memory.’ Therefore, familiar motions might be more appropriate for physical therapy in patients with apparent dementia.

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Learning points

17
18

▸ The patient had reduced working memory, and consequently
she required a long time to remember instructions for
isometric contraction exercise of the quadriceps.
▸ The MRI revealed deep white matter changes.
▸ The 18f-fluoro-D-glucose-positron emission tomography
showed reduced metabolism in the bilateral frontal lobes,
and particularly in the dorsolateral prefrontal area, anterior
cingulate and orbital area.

19
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21

22
23

Contributors KT is the physical therapist, and KM and MN are the neurologists for
the case. NT was involved in writing the article and was the physicist who
performed positron emission tomography.

6

24

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Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

Reminder of important clinical lesson

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Takeda K, et al. BMJ Case Rep 2013. doi:10.1136/bcr-2013-008577

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