J Neurol Neurosurg Psychiatry 1999;66:233–237

233

SHORT REPORT

Pure apraxic agraphia with abnormal writing
stroke sequences: report of a Japanese patient with
a left superior parietal haemorrhage
Mika Otsuki, Yoshiaki Soma, Toshiko Arai, Atsuko Otsuka, Shoji Tsuji

Cerebrovascular
Division, Department
of Internal Medicine,
National
Cardiovascular Center,
Japan
M Otsuki
Department of
Neurology, Brain
Research Institute,
Niigata University,
Japan
Y Soma
S Tsuji

Abstract
A 67 year old Japanese male patient had
pure agraphia after a haemorrhage in the
left superior parietal lobule. He developed
diYculty in letter formation but showed
no linguistic errors, consistent with the
criteria of apraxic agraphia. He manifested a selective disorder of sequencing
writing strokes, although he was able to
orally state the correct sequences. The
patient’s complete recovery after 1 month,
without new learning, showed that he had
manifested a selective disorder of writing
stroke sequences. These findings indicate
that the final stage of the execution of
writing according to acquired sequential
memory shown as a stroke sequence can
be selectively disturbed, and should be
considered to be distinct from the ability
of character imagery and the knowledge of
the writing stroke sequence itself. This
case also indicates that the left superior
parietal lobule plays an important part in
the execution of writing.
(J Neurol Neurosurg Psychiatry 1999;66:233–237)
Keywords: pure apraxic agraphia; left superior parietal
lobule; writing stroke sequences

Correspondence to:
Dr Mika Otsuki,
Cerebrovascular Division,
Department of Internal
Medicine, National
Cardiovascular Center, 5-7-1
Fujishirodai, Suita, Osaka,
565-8565, Japan. Telephone
0081 6 833 5012; fax 0081 6
872 7486.

Pure agraphia is an impairment in writing unaccompanied by any other relevant language
disorder,1 which occurs in association with
lesions in the frontal lobe,2 superior parietal
lobule,3–5 temporal lobe,6 left caudate nucleus
and internal capsule,7 and left thalamus.8 9
Regarding the type of pure agraphia and the
lesions, the parietal lobe is considered a
candidate site of the causative lesion for
disorders of spatial and kinesthetic movements
of writing3 4; however, the relation between the
type of agraphia and other lesions remains
uncertain. We herein report a case of pure
agraphia after a haemorrhage in the left superior
parietal lobule in a Japanese patient, who
showed a characteristic impairment of writing,
and we discuss the symptoms and the mechanism of pure agraphia after a left parietal lesion.

Received 30 April 1998 and
in revised form
10 August 1998
Accepted 25 August 1998

Case description
A 67 year old, right handed, university
educated Japanese male bank clerk was admit-

Department of Speech
Therapy, Takeda
General Hospital,
Japan
T Arai
A Otsuka

ted to Takeda General Hospital on 12 October
1993. He had been in good health without any
relevant history of disease, but was subsequently found to have hypertension. On the
evening of 12 October he noted sudden weakness in his right arm while he was at his oYce.
His colleagues noted at that time that he
answered their questions irrelevantly and they
brought him to the hospital. A neurological
examination showed him to be alert, but disoriented as to time and place. The cranial nerves
were all intact, and he showed no paresis in the
limbs, and no pathological reflexes or sensory
deficits. By the next day he had become well
oriented, but he became aware of an impairment in his writing. Brain MRI performed 22
days after onset (fig 1) disclosed a circumscribed haemorrhage in the left superior
parietal lobule. Seventeen days after onset,
N-isopropyl-(123I)-p-iodoamphetamine single
photon emission computed tomography
(SPECT) disclosed decreased blood flow
corresponding to the region showing a haemorrhage, as disclosed by MRI.
Neuropsychological assessment
From the onset, the patient’s speech was fluent
and well articulated, and he showed no
orofacial apraxia. The western aphasia
battery,10 Japanese version11 was administered
within 1 week after onset, and disclosed no
aphasic findings or reading disability except for
a writing impairment. On the revised Wechsler
adult intelligence scale (WAIS-R), administered 13 days after onset, the patient showed a
verbal IQ of 109, performance IQ of 100, and
full scale IQ of 105. Regarding the praxis
examined during the first week after onset, he
was able to make meaningful gestures such as
beckoning, waving goodbye, tooth brushing,
pretended tool use, and pantomime on verbal
command and on imitation; he was also able to
imitate meaningless gestures made by the
examiners, and he could use tools accurately,
which indicated that he had no impairment in
praxis such as ideomotor apraxia or ideational
apraxia. He was able to imitate simple finger
patterns using either hand, and he showed no
clumsiness. He was able to copy cubic and
Rey-Osterreith’s designs without any problem,
with the normal strategy employed to copy, and

234

Otsuki, Soma, Arai, et al

Figure 1 T2 weighted brain MR axial images (TR=3000, TE=90) of the patient obtained 22 days after onset. A circumscribed haemorrhage in the left
superior parietal lobule is seen. Scattered white matter lesions indicate the ischaemia within the white matter after hypertension.

obtained a normal score on the block design
test (score of 11 on the WAIS-R), which
indicated that he had no constructional disturbance. There was no spatial disturbance, optic
ataxia, or visual agnosia.
We administered writing tests 18 days after
onset: the dictation and transcription of
educational Kanji (morphograms12), and the
same words written in Kana (syllabograms12).
We used the easiest Kanji, selected at random
from among educational samples for pupils at
elementary school level.
Results
The results are summarised in the table and
writing samples by the patient are shown in figure 2. Before any further description, it is necessary to explain the Japanese writing system.
There are two systems of writing in Japanese;
Kanji
(morphograms12)
and
Kana
(syllabograms12). Kanji often have very complicated shapes, achieved with as many as 10–20
strokes, and many Kanji thus require a
particular writing stroke sequence. Figure 2, A,
B, and C are examples of Kanji. Thus it is a
fundamental educational subject for Japanese
pupils to learn the stroke sequences of Kanji.
They learn them by practicing the sequences
repeatedly, not only through knowledge but
also using sequential movement memory. Kana
are much simpler than most Kanji; Kana are
generally two to four stroke symbols of mora
(in the Japanese language, the ultimate minimum unit of a sound corresponds to a mora,
which can in turn correspond to one Kana letter) such as “ro” or “bo” (fig 2, D shows two
Kana). Examples of both the correct sequences
of strokes for Kanji or Kana, which were shown
by the patient after his recovery, and the
patient’s writing with unusual stroke sequences
during his morbid period are shown in fig 2.
In addition to the ill shaped letter formation,
the patient characteristically showed an unusual sequence of strokes for forming Kanji or
Kana, although he was able to eventually arrive
at the correct formation. The patient complained of his impairment of writing as follows:
“My hand slips, although I know how to write.”
This symptom was observed in the writing of

both Kanji and Kana, equally on spontaneous
writing, dictation, and transcription. He himself noticed that his stroke sequences were
strange, and he was able to express orally without any diYculty how the sequence of strokes
should proceed and how he used to perform
the sequence before the haemorrhage. Therefore, his knowledge of the sequence of writing
strokes seemed to be preserved. He sometimes
succeeded in correcting his mistakes, but not
always. He showed no spelling errors in his
writing, and he was perfectly able to select correct Kanji or Kana from among the samples
and make words and sentences.
At the re-examination 1 month after onset,
in the same writing tests administered earlier,
the patient was able to write correctly all of the
Kanji and Kana tested with the correct
sequence of writing strokes, without new
learning, and he has never shown an unusual
stroke sequence in writing since then. In a
Results of reading and writing examinations

Reading (administered 17 days
after onset):
Administered numbers
Correct answers
Writing (administered 18 days
after onset):
Administered numbers
Correct answers
A
B
C
D

Kanji

Kana*

50
50 (100%)

50
50 (100%)

50

50

38 (76%)
10 (20%)
1 (2%)
1 (2%)

38 (76%)
9 (18%)
3 (6%)
0 (0%)

(A) Correct shapes with a correct sequence of strokes; (B) correct shapes with an unusual sequence of strokes; (C) bad
formation; (D) no recall
* Regarding the examinations of Kana, the administered numbers are not the numbers of Kana letters but are Kana words,
which consist of several Kana letters. We assessed the patient’s
performance according to the existence of mistakes, which
means that even if the patient showed an incorrect response in
one Kana letter, we assessed the entire word as an incorrect
response, and the patient was assessed as giving a normal answer
only when he was able to complete whole words with completely
correct letter formation. We used Kana for the word
examinations because the number of Kana letters is limited,
only 46 in all, compared with the standard elementary school
vocabulary level of 1000 Kanji. We also hoped to examine the
patient’s ability to write sequential movements which demand a
certain flow, so it seemed preferable to adopt words to each letter. Thus, the patient’s scores on the Kanji and Kana examinations results cannot be directly compared for the degree of the
writing disorder.

Pure apraxic agraphia with abnormal writing stroke sequences

235

Figure 2 Top: writing samples of the patient show a poorly formed Kana word. He had tried to rewrite the same word,
which consists of three Kana letters, “A-i-zu” (which is the name of the city in which the patient lives) repeatedly from the
top to the bottom as the arrow indicates, but he was not able to complete it (11 days after onset). Bottom: the patient’s
unusual order of writing strokes at dictation (18 days after onset). The right side of each column shows the correct sequence
used to make the complete character, shown at the bottom of each column. The patient executed the writing in the order
indicated by the arrow in the left hand columns. (A) This character (Kanji), for aviation, was not completed correctly. (B)
This character (Kanji), for fly, was completed correctly, but with an unusual order of writing strokes. (C) This character
(Kanji), for part of the patient’s name, was also made with an unusual sequence. (D) These two letters (Kana), for
“ro-bo”, part of the word “robot”, were eventually completed correctly, but with an unusual sequence order.

re-examination of the WAIS-R, the patient
showed a verbal IQ of 92, a performance IQ of
105, and a full IQ of 98.
Discussion
We have described a patient who manifested an
impairment in only writing after a circumscribed haemorrhage in the left superior
parietal lobule, without any other symptoms
such as aphasia, alexia, agnosia, limb clumsiness, ideomotor apraxia, ideational apraxia, or
constructional disturbance. He showed no
other abnormal findings which could possibly
cause a writing disturbance, such as dementia
or general memory disturbance. His writing
impairment persisted for a month and cannot
be simply ascribed to an acute confusional state
and cannot be interpreted as transient and
negligible, because he was able to perform

other examinations without any abnormality
during the same period and there is no confusional state known which shows such a selective
disorder persisting for 1 month. In addition,
the patient’s WAIS-R re-examination showed
almost the same IQ score, indicating that the
patient’s writing impairment cannot be ascribed to general mental deterioration during
the morbid period. Therefore, the patient’s
symptom can be interpreted as a focal sign after
the onset of haemorrhage, and it was consistent
with the criteria for pure agraphia.1
Previous neuropsychological assessments of
pure agraphia have disclosed that it can be
classed into two types: in “linguistic” agraphia,
the patients manifest spelling errors, and in
“apraxic” agraphia, they manifest abnormal
letter formation. Although apraxic agraphia is
termed “apraxic,” it is not accompanied by

236

Otsuki, Soma, Arai, et al

limb apraxia or a constructional disturbance.
Baxter and Warrington13 used the term “pure”
apraxic agraphia to identify the symptom of
writing disturbance appearing in the absence of
a disturbance of spelling, reading, or other
general language problems, and importantly,
occurring in the absence of major praxic or
visual-constructional diYculties. Although the
early reports of patients with apraxic agraphia
disclosed the fact that writing apraxia and limb
apraxia could be distinct,14 15 these patients had
atypical cerebral dominance. For this reason
the authors considered that the dissociation of
writing apraxia and limb apraxia could be due
to the atypical cerebral dominance. Subsequently Baxter and Warrington13 issued the
first report describing a patient with typical
cerebral dominance who seemed to have
apraxic agraphia, and they postulated that their
patient’s inability arose at the level which
specifies the motor sequences or “graphic
motor pattern,” and termed it “ideational
agraphia.” Their report indicated that selective
writing apraxia can also occur in a patient with
typical cerebral dominance.
Our patient showed pure agraphia with a
preserved ability for spelling, and he was able
to select letters or characters correctly, all of
which indicate that he had no linguistic
impairment. He was able to make excellent
copies of cubic and Rey-Osterreith’s designs
and had a normal score on block design tests,
results which show that he had no visual
constructional impairment. He showed ill
shaped letter formation without any other
inability, and these findings disclosed his
symptom pattern to be similar to those of the
patients described as having apraxic agraphia
in the previous reports.4 13 15 16
The most characteristic of our patient’s
impairment was the conspicuous, unusual, and
incorrect writing sequence strokes. As shown in
fig 2, Japanese Kanji have complicated stroke
sequences and, thus, if people who are not
familiar with Kanji, try to transcribe such a
character, they would not know which line to
write first and which should be second, etc.
Our patient wrote Kanji and Kana with
unusual stroke orders, although he was able to
write the complete Kanji or Kana. He wrote
each Kanji or Kana as if he were transcribing
an unfamiliar foreign shape, both at dictation
and transcription. Naturally, the degree of
achievement in mastering the correct writing
stroke order depends on the individual person,
and some Japanese people fail to master them
and habitually use some idiosyncratic stroke
sequences. However, we cannot ascribe our
patient’s unusual stroke orders to low achievement or to personal habit for two reasons; one
is because he could orally state how the correct
sequence of strokes should proceed even when
he was not able to perform the strokes, and
because he recovered from his impairment
after a month, without new learning, showing
perfectly correct sequences of strokes for the
writing of each Kanji and Kana tested earlier. It
is reasonable to assume that he simply
recovered to his premorbid level, as it would
have been impossible for him to learn anew all

of the correct stroke sequences for each letter
or character in a month.
There are few reports in the western
literature of patients with pure agraphia showing an unusual stroke sequence. We suspect
that the nature of the Japanese writing system
disclosed the patient’s disturbance more conspicuously. In the Japanese literature, Ishiai et
al17 reported pure agraphia due to a left parietal
lobe infarction in a patient, who showed
unusual sequences of writing strokes, which
seems similar to the impairment of our patient.
Our patient was able to orally state not only the
correct spelling but also the correct sequences
of writing strokes for all Kanji and Kana tested,
which indicates that his disturbance was not
one of memory of the stroke order as
knowledge itself but rather a disturbance in the
process of the execution of writing as sequential memory.
Rothi and Heilman16 postulated the existence of a graphemic area that is responsible for
guiding motor programming in grapheme production. Roeltogen and Heilman14 described a
patient who was unable to write any formed
graphemes despite a preserved ability to spell
aloud, whose disorder was thought to be a disconnection of output from the graphemic area.
This disorder seems relevant to that of our
patient. In addition to this disorder, our patient
showed the unusual writing stroke sequences
even when his writing did not show poor
formation, and he could not improve by copying. This indicates that the disorder arose at the
final stage of motor output, which involves
both spontaneous writing and copying. Cray
and Heilman18 presented a case of pure apraxic
agraphia in which defective letter imagery was
evident, and they proposed the possibility of
two regulation sites in the graphemic area, one
for letter imagery and the other for motor
transcoding. Our patient presented evidence of
a selective disorder of the second site: a disorder of motor transcription without letter
imagery disorder.
Regarding the causative lesions for apraxic
agraphia, Alexander et al3 reported the lesion
localisation as the superior parietal lobule.
Kapur and Lawton19 hypothesised that parietal
agraphia is due to a memory diYculty for the
motor movements associated with letters. In
the parietal area, we hypothesise that a lesion
restricted to the left superior parietal lobule can
cause a selective impairment of the execution
of writing sequence, manifested as an abnormal order of writing strokes. This would be
particularly conspicuous in a Japanese patient,
because Japanese characters and letters require
certain complicated stroke sequences, a feature
which demands much of sequential memory.
1 Roeltgen DP. Agraphia. In: Heilman KM, Valenstein E, eds.
Clinical neuropsychology, 3rd ed. New York: Oxford University Press, 1993;66.
2 Exner S. Untersuchungen uber die Lokalisation der Funktionen
in der Grosshirnrinde des Menschen. Wien: W Braumuller,
1881.
3 Alexander MP, Fisher RS, Friedman R. Lesion localization
in apractic agraphia. Arch Neurol 1992;49:246–51.
4 Auerbach SH, Alexander MO. Pure agraphia and unilateral
optic ataxia associated with a left superior parietal lobule
lesion. J Neurol Neurosurg Psychiatry 1981;44:430–2.

237

Pure apraxic agraphia with abnormal writing stroke sequences
5 Basso A, Taborelli A, Vignolo LA. Dissociated disorders of
speaking and writing in aphasia. J Neurol Neurosurg
Psychiatry 1978;41:556–63.
6 Rosati G, de Bastiani P. Pure agraphia: a discrete form of
aphasia. J Neurol Neurosurg Psychiatry 1979;42:266–9.1]
7 Laine TN, Marttila RJ. Pure agraphia: a case study.
Neuropsychologia 1981;19:311–6.
8 Aiba E, Soma Y, Aiba T, et al. Two cases of pure agraphia
developed after thalamic hemorrhage. Brain and Nerve
(Tokyo) 1991;43:275–81. (In Japanese.)
9 Sugishita M, Ishijima B, Hori T, et al. Pure agraphia after
CM-thalamotomy. Clinical Neurology (Tokyo) 1973;13:
568–74.
10 Kertesz A. The western aphasia battery. New York: Grune
and Stratton, 1982.
11 Sugishita M. The western aphasia battery (Japanese ed).
Tokyo: Igakushoin, 1986.
12 Iwata M. Kanji versus Kana; Neuropsychological correlates
of the Japanese writing system. TINS 1984;8:290–3.

13 Baxter DM, Warrington EK. Ideational agraphia: a single
case study. J Neurol Neurosurg Psychiatry 1986;49:369–74.
14 Roeltgen DP, Heilman KM. Apractic agraphia in a patient
with normal praxis. Brain Lang 1983;18:35–46.
15 Margolin DI, Binder L. Multiple component agraphia in a
patient with atypical cerebral dominance: an error analysis.
Brain Lang 1984;22:26–40.
16 Rothi LJ, Heilman KM. Alexia and agraphia with spelling
and letter recognition abilities. Brain Lang 1981;12:1–13.
17 Ishiai S, Sugishita M, Lee E, et al. Process of writing in
alexia with agraphia and pure agraphia. Shitsugosho Kenkyu
(Higher brain function research) 1993;13:264–271. (In Japanese.)
18 Crary MA, Heilman KM. Letter imagery deficits in a case of
pure apraxic agraphia. Brain Lang 1988;34:147–56.
19 Kapur K, Lawton NF. Dysgraphia for letters: a form of
motor memory deficit. J Neurol Neurosurg Psychiatry 1983;
46:573–5.

NEUROLOGICAL STAMP

Multiple sclerosis
The recognition of multiple sclerosis as a clinical entity
diVerent from other movement disorders or spinal
paraplegias was made by Charcot in 1868. Previously multiple sclerosis had been repeatedly confused with paralysis
agitans. It was Charcot who made the first definitive
pathological description that distinguished the two diseases. The pathological lesions of multiple sclerosis, probably first illustrated 30 years earlier in 1838 by Robert
Carswell, were those of an unnamed French patient. Carswell, a Scotsman, held the inaugural chair of pathology at
London University. (Compston A. The 150th anniversary
of the first depiction of the lesions of multiple sclerosis. J
Neurol Neurosurg Psychiatry 1988; 51:1249-52.) Until the
mid-1960s little was known about the disordered physiology produced by demyelination. In 1963 Professor Ian
McDonald demonstrated that electrical signs of conduction block developed abruptly at the junction of normal
and demyelinated parts of nerves. McDonald and Sears, in
1969, showed that conduction block occurred at the margin of the lesions produced in the posterior columns of cats
and that portions of the nerve fibres distal to the block
retained their ability to conduct impulses. One hundred
and forty three years after Carswell’s illustration the ability
of NMR to disclose abnormalities with multiple sclerosis

on a scale not previously seen, except at necropsy, was
demonstrated. The potential of NMR to assist in the diagnosis of MS was established. (Young IR et al. Lancet 1981;
ii: 1063-5.)
In 1962 Monaco produced this stamp showing the sun,
flowers, and a chest filled with hope (Stanley Gibbons 151,
Scott 506). It was another 30 years before realistically
hopeful therapies for the disorder began to emerge.
L F HAAS