Parietal Dysgraphia: Characterization of Abnormal Writing Stroke Sequences, Character Formation and Character Recall

Abstract

To characterize various dysgraphic symptoms in parietal agraphia.
We examined the writing impairments of four dysgraphia patients from parietal lobe lesions using a special writing test with 100 character kanji (Japanese morphograms) and their kana (Japanese phonetic writing) transcriptions, and related the test performance to a lesion site.
Patients 1 and 2 had postcentral gyrus lesions and showed character distortion and tactile agnosia, with patient 1 also having limb apraxia. Patients 3 and 4 had superior parietal lobule lesions and features characteristic of apraxic agraphia (grapheme deformity and a writing stroke sequence disorder) and character imagery deficits (impaired character recall). Agraphia with impaired character recall and abnormal grapheme formation were more pronounced in patient 4, in whom the lesion extended to the inferior parietal, superior occipital and precuneus gyri.
The present findings and a review of the literature suggest that: (i) a postcentral gyrus lesion can yield graphemic distortion (somesthetic dysgraphia), (ii) abnormal grapheme formation and impaired character recall are associated with lesions surrounding the intraparietal sulcus, the symptom being more severe with the involvement of the inferior parietal, superior occipital and precuneus gyri, (iii) disordered writing stroke sequences are caused by a damaged anterior intraparietal area.

Full text

Behavioural Neurology 18 (2007) 99–114 99
IOS Press
Parietal dysgraphia: Characterization of
abnormal writing stroke sequences, character
formation and character recall
Yasuhisa Sakurai
a,b,∗
, Yoshinobu Onuma
a
, Gaku Nakazawa
a
, Yoshikazu Ugawa
b
, Toshimitsu Momose
c
,
Shoji Tsuji
b
and Toru Mannen
a
a
Department of Neurology, Mitsui Memorial Hospital, Tokyo, Japan
b
Department of Neurology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan
c
Department of Radiology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan
Abstract. Objective: To characterize various dysgraphic symptoms in parietal agraphia.
Method: We examined the writing impairments of four dysgraphia patients from parietal lobe lesions using a special writing test
with 100 character kanji (Japanese morphograms) and their kana (Japanese phonetic writing) transcriptions, and related the test
performance to a lesion site.
Results: Patients 1 and 2 had postcentral gyrus lesions and showed character distortion and tactile agnosia, with patient 1 also
having limbapraxia. Patients 3 and 4 had superior parietallobule lesions and features characteristic of apraxic agraphia (grapheme
deformity and a writing stroke sequence disorder) and character imagery deficits (impaired character recall). Agraphia with
impaired character recall and abnormal grapheme formation were more pronounced in patient 4, in whom the lesion extended to
the inferior parietal, superior occipital and precuneus gyri.
Conclusion: The present findings and a review of the literature suggest that: (i) a postcentral gyrus lesion can yield graphemic
distortion (somesthetic dysgraphia), (ii) abnormal grapheme formation and impaired character recall are associated with lesions
surrounding the intraparietal sulcus, the symptom being more severe with the involvement of the inferior parietal, superior
occipital and precuneus gyri, (iii) disordered writing stroke sequences are caused by a damaged anterior intraparietal area.
Keywords: Apraxic agraphia, parietal pure agraphia, intraparietal sulcus, limb apraxia, somatosensory area
1. Introduction
Agraphia caused by lesions of the parietal lobe
presents as three types with different anatomical sub-
strates: alexia with agraphia from an angular gyrus
lesion, pure agraphia from a superior parietal lobule
lesion and agraphia with conduction aphasia [5,32].
Little is known about the clinical features of pure
agraphia from a superior parietal lobule lesion [2,3];
the patients make phonemic paragraphia consisting of
∗
Corresponding author: Yasuhisa Sakurai, MD, PhD., Depart-
ment of Neurology, Mitsui Memorial Hospital, 1, Kanda-Izumi-cho,
Chiyoda-ku, Tokyo 101-8643, Japan. Tel.: +81 3 3862 9111; Fax:
+81 3 5687 9765; E-mail: ysakurai-tky@umin.ac.jp.
substitutions and omissions. A lesion in the superior
parietal lobule [1] or surrounding the intraparietal sul-
cus [30] is known to cause apraxic agraphia, which is
characterizedby difficultyin forminggraphemes. This
condition produces inversions and distortions, despite
normal sensorimotor function and relatively preserved
oral spelling and typing using anagram letters [11].
Pure agraphia in general differs from apraxic agraphia
in that patients usually make well-formed graphemes
(written letters) [32]. One patient reported as having
pure agraphia from a superior parietal lobule lesion [2]
showed poorly formed graphemes and thus should be
regarded as having apraxic agraphia. However, it re-
mains unknown whether parietal pure agraphia and
apraxic agraphia share the same lesion.
ISSN 0953-4180/07/$17.00  2007 – IOS Press and the authors. All rights reserved

100 Y. Sakurai et al. / Parietal dysgraphia
The Japanese writing system uses two distinct
scripts: kanji (morphograms or ideograms, originally
adopted from Chinese characters) and kana (Japanese
phoneticwritingorsyllabograms,originallytakenfrom
kanji characters). Some kanji characters with complex
figures require many writing stroke sequences. Prima-
ry school students learn the order of kanji and kana
character writing stroke sequences. Due to the use of
these dual systems, agraphia in Japan presents itself in
somewhat unique and pronounced ways. For example,
(1) agraphia of kanji resulting from impaired character
recall (lexical or orthographic agraphia) occurs in le-
sions of the posterior inferior temporal cortex [19,36,
41], angular gyrus [14,17,25,38],superior parietal lob-
ule [17,23] and posterior middle frontal gyrus [35]; (2)
paragraphia of kana (phonological agraphia) occurs in
lesions of the supramarginalgyrus [37,43] and the pos-
terior part of the middle and inferior frontal gyri [35];
and (3) Japanese apraxic agraphia patients with a su-
perior parietal lobule lesion show disordered stroke se-
quences and distortions in writing kanji [14,29].
On the basis of the above findings (1) and (2), we
previouslyhypothesizedthat visual images ofkanjiand
kana words (and letters) are stored in the posterior in-
ferior temporal cortex (and also the angular/lateral oc-
cipital gyri in case of kana characters) and travel via
the angular gyrus and superior parietal lobule to the
frontal motor and premotor areas (orthographic route,
formerly “morphologic route”) [35], whereas phono-
logical information of words and letters goes from the
primaryauditory cortex and the posterior superiortem-
poral gyrus to the angular and supramarginal gyri and
joinsthearcuatefasciculustotravelto the frontalmotor
and premotor areas (phonological route). A phoneme-
linked visual image of kana or a syllable is accessed
in the angular gyrus and the adjoining lateral occipital
gyri and then the visual information of kana joins the
orthographicroute. Kanji charactersthat are graphical-
ly complex and have multiple stroke sequences depend
more on the orthographic route, whereas kana charac-
tersthatlinkdirectlytophonemesandhaveagraphical-
lysimpleconfigurationdependless on the orthographic
route. This hypothesis is consistent with recent neu-
roimaging findings (see Fig. 1 of Nakamura et al. [26])
that(i) kanji character writing and recallactivatedmore
extensiveareas inthe posteriorinferior temporalcortex
andsuperior parietal lobulethan kana characterwriting
and recall, and (ii) kanji writing and recall activated
an extensive area of the posterior middle frontal gyrus
(end of the orthographic pathway, Area 6), whereas
kana writing and recall activated a limited area of the
frontal operculum (end of the phonological pathway,
Area 44/45). Recent neuropsychologicalfindings from
Western countries also support the view that the poste-
riorinferiortemporal cortexis a site fortheorthograph-
ic lexicon for words [31] and additionally the posterior
middleand inferiorfrontalgyri(Areas 44/45and6)and
angular gyrus (Area 39) are concerned with accessing
orthography [12,13].
A weak point of this hypothesis is that it does not
take into account the features of apraxic agraphia,
i.e. grapheme deformity and the above (3), following a
superior parietal lobule lesion. Thus, it should be de-
termined which lesion in the superior parietal lobule is
responsibleforgraphemedeformity,disorderedwriting
stroke sequences, and impaired recall of word images,
respectively. Here, we report four patients with pari-
etal writing impairment: isolated character deformity
with or without limb apraxia, agraphia with character
deformityand a stroke sequencedisorder,and agraphia
with a stoke sequence disorder and marked character
deformity and imagery deficits (impaired character re-
call). We correlated the writing symptoms with the
lesions and suggested anatomical substrates for these
disturbances.
2. Materials and methods
2.1. Patient profiles
Patient 1. In December 2001, a 36-year-old natu-
rally left-handedman (laterality quotient by Edinburgh
Handedness Inventory [28], -63), senior high school
graduate and office worker trained to write with both
hands in primary school, noted numbness of the left
arm. He could not grasp anything. He was admitted
to our hospital having been diagnosed with a cerebral
infarction on CT. Neurological and neuropsychologi-
cal examinations showed weakness of the left upper
extremity, paresthesia with cheiro-oraltopographythat
affected the left palm and oral corner, pseudoatheto-
sis of the third to fifth fingers, tactile agnosia resulting
from impaired combined sensations (texture recogni-
tion, two-point discrimination and graphesthesia) and
limb apraxia of the left hand. His digit span forward
score was 6, and backward 4. In two weeks his grip
strength recovered,paresthesia was limited to the third
tofifthfingers,andhe couldbarelywrite,althoughlimb
apraxia still persisted.
The Western Aphasia Battery (WAB; Japanese edi-
tion) administered 13 days after onset showedno apha-

Y. Sakurai et al. / Parietal dysgraphia 101
Fig. 1. Abnormal writing postures in patient 1 with “somesthetic dysgraphia.” Patient 1 wrote characters holding the pencil with the intact left
thumb and index finger. He had tactile agnosia resulting from impaired combined sensations and limb apraxia in the left hand.
sia, but he wrote characters poorly (Table 1). He held
the pencil in an awkward manner and wrote slowly
and laboriously with the intact thumb and index finger
(Fig. 1), which resulted in deformities of the written
characters such as elongation and interruption of the
lines. He formedbetter characterswhen copyinga sen-
tence than when writing in response to dictation. The
patient could naturally hold the pencil and write kanji
and kana words with the right hand without charac-
ter distortion. Limb apraxia and tactile agnosia disap-
peared in a month and the left hemiparesis recovered,
butparesthesia of the third to fifth fingersand impaired
two-point discrimination still continued four months
after onset.
MRI seven days after onset revealed high intensi-
ty areas in the right postcentral gyrus posterolateral
to the precentral knob (cortical hand area above the
operculum) [46], cortical and subcortical structures in
the supramarginal and posterior middle temporal gyri
(Fig. 2-1). There was another high intensity area in
the right middle occipital gyrus that suggested an old
infarction. Carotidangiographydisclosed an occlusion
ofthehorizontalportion(parssphenoidalis)oftheright
middle cerebral artery.
Patient 2. In December 2001, a 74-year-old right-
handed man, university graduate and retired office
worker, noticed his right arm was weak and consulted
our department. He was diagnosed as having a cere-
bral hemorrhagein the left parietal lobe on CT. He was
admitted to the Department of Neurology at our hospi-
tal. On admission the patient showed slight weakness
and paresthesia of the right arm, and tactile agnosia of
the right handresulting from deficient combinedsensa-
tions(texturerecognition,two-pointdiscriminationand
graphesthesia). He stated that everything he touched
felt metallic and hard. There was no limb apraxia. He
wrote kanji characters poorly,but recoveredthis ability
considerably within ten days.
WAB ten days after onset showed no aphasia, but
the patient wrote sentences slowly: he wrote only two
sentencesin threeminuteswhenwritingspontaneously,
which resulted in a lower score for writing (Table 1).
Some kanji and kana characters were poorly formed
when writing spontaneously and writing in response to
dictation,butmuchimprovedwhencopyinga sentence.
One month after onset, paresthesia was limited to the
third to fifth fingers and pseudoathetosis was observed
in the fourth finger. Writing impairment recovered to
within the normal range three months after onset.
MRI eight days after onset revealed a high intensity
on T1- and a low intensity on T2-weighted images in
the localized area of the left postcentral gyrus posteri-
or to the precentral knob (Fig. 2-2). There was mild
enlargement of the left lateral ventricle.
Patient 3. In September 1996, a 58-year-old right-
handedman, seniorhighschoolgraduateand tie maker,
found that he could not move his right arm, had lost
his sense of touch with it, and felt as if it was another
person’s. Ten minutes later when the motor weakness
and sensory disturbance were recovered to some ex-
tent, he misspelledJapanese characters, eventhoughhe
could recall their visual images. When he referred to a
textbook, he could copy the characters correctly. Two
days later, he couldnot knot a tie, andfelt as if his right
leg was covered with thin cotton. The patient was ad-
mitted to the Department of Neurology, University of
Tokyo Hospital having been diagnosed with a cerebral
infarction in the left parietal lobe on CT. Neurologi-

102 Y. Sakurai et al. / Parietal dysgraphia
Table 1
Standard neuropsychological test scores
Patient (age) 1 (36) 2 (74) 3 (58) 4 (58)
WAIS-R
Verbal IQ 89 107 116 94
Performance IQ 73 94 108 65
Picture Completion 6 11 12 8
Picture Arrangement 5 6 12 6
Block Design 7 11 9 3
Object Assembly 9 8 11 3
Digit Symbol (raw score) 4 (35) 9 (29) 12 (50) 4(15)
WA B
Spontaneous speech
Information content (/10) 10 10 10 10
Fluency (/10) 10 10 10 10
Naming total (/10) 9.9 8.8 9.7 8.9
Repetition (/10) 10 10 9.8 10
Comprehension total (/10) 10 10 9.95 9.8
Reading total (/10) 9.5 10 9.2 8.8
Recognition of orally spelled kanji (/6)
#
261*0*
Oral spelling of kanji characters (/6)
#
56 30*
Writing total (/10) 10 8.6 8.6 3.15
Copying (/10) 10 10 10 10
Kanji word writing from dictation (/6) 6 6 4.5 1*
Kana word writing from dictation (/6) 6 6 5.5 0*
Dictated kana characters (/5) 5 5 5 0*
*Subtest score is more than 2SD below the normal mean [42].
#
Recognition of orally spelled kanji denotes that a patient is asked to guess a kanji
character (e.g.
[naku], sing) from the two components ( [kuchi], mouth, and [tori],
bird) spoken by the examiner. Oral spelling of kanji characters denotes that a patient
is asked to describe two components (e.g.
[onna], woman, and [ichi], city) of a
kanji character (
[ane], sister) spoken by the examiner. These two tasks require mental
imagery of a kanji character.
cal and neuropsychological examinations at this time
showed no motor or sensory deficit, but impairments
in short-term memory (digit span forward score was
four), writing and mental arithmetic.
WAB administered four days after onset showed
agraphiaandanimpairmentoffinger identification(Ta-
ble 1). Writing errors included an impairment of kanji
character recall, sometimes leading to neologisms, and
literal paragraphia for kana. He used trial and error,
particularly when writing kanji characters. Recogni-
tion of orally spelled kanji characters was significant-
ly poor (for an example of this test, see the footnote
of Table1), suggesting letter imagery deficits (impaired
character recall). Copying of a sentence was perfect
and orthographically improved compared to dictation,
but he wrote stroke by stroke, referring to the sample.
The patient complained that he could not write char-
acters as he imagined. We did not examine his typing
performance. There was no apraxia. Knotting a tie be-
came possible as he practiced again. Calculation was
slightly impaired in another calculation test between
two digits and one digit [37] (mental arithmetic,38/40;
written calculation, 39/40). Impaired short-term mem-
oryandacalculia recoveredto a normal levelafter three
months, but the patient stated that he had difficulty
writing characters over the next few years.
MRI one month after onset disclosed a high intensi-
ty area posterior to the left postcentral sulcus, includ-
ing the superior parietal lobule and part of the supra-
marginalgyrus, that extendeddeep along the intrapari-
etal sulcus to the left lateral ventricle on T2-weighted
images (Figs 2–3). There were also small high inten-
sity spots in the central semiovale on both sides and
mildenlargementofthe lateral ventriclesthat was more
pronounced on the left.
Patient 4. In July 2001, a 58-year-old right-handed
man, retired storekeeper, noticed convulsive move-
ments in the right extremities and found difficulty writ-
ing. He could not make discrete finger movements or
reach a glass on a table. He had sustained a cerebral
hemorrhage in the left occipital lobe in January 1998
anddevelopedrighthomonymoushemianopiaandtran-
sient alexia. CT showed a low density area around the
old infarction in the left occipito-parietal area. The
patient was admitted to the Department of Neurology
at our hospital having been diagnosed with a cerebral

Y. Sakurai et al. / Parietal dysgraphia 103
Fig. 2. MRI axial and coronal images of patients 1 to 4. Number corresponds to the patient number. Axial slices are at the level of upper part of
the lateral ventricle and the intraparietal sulcus, and coronal slices area at the level of the posterior horn of the lateral ventricle and the angular
gyrus. 2-1: High intensity areas were noted in the right postcentral gyrus posterolateral to the precentral knob, cortico-subcortical structures in
the supramarginal gyrus on T2-weighted images (arrowhead, Time of repetition [TR] / Time of echo [TE] = 7999msec/104msec). These lesions
were identified with diffusion-weighted images. On the coronal view, the postcentral gyrus lesion extended deep to the lateral ventricle (TR/TE
= 4000/83). 2-2: A low intensity area suggestive of hemorrhage was localized in the left postcentral gyrus posterior to the precentral knob on
T2-weighted images (arrowhead, TR/TE = 7999/101). On the T1-weighted planes, a high-intensity hemorrhage was noted over the posterior
horn of the lateral ventricle (TR/TE = 500/14). 2-3: A high intensity area posterior to the postcentral sulcus extended deep along the intraparietal
sulcus to the lateral ventricle on T2-weighted axial images (TR/TE = 3500/96). 2-4: A thin high intensity area was located in the occipital and
parietal lobes that extended anteriorly to the postcentral sulcus, surrounding an old infarction (thick intensity area) in the medial occipital lobeon
T2-weighted axial images (TR/TE = 7999/101). The new lesion involved the superior parietal lobule, angular gyrus and precuneus that extended
posteriorly to the superior occipital gyrus on coronal images (TR/TE = 4000/84).
infarction. Neurological and neuropsychological ex-
aminationsshowed(1) right homonymoushemianopia,
later confirmed by Goldmann perimetry, (2) Barr
´
e’s
handpronationsignoftherightupperextremityandthe
right extensor plantar response, (3) agraphia for kanji
and kana caused by impaired character recall, (4) an
impairment of short-term memory (digit span forward
score was four), (5) acalculia, and (6) a visually guided
reachingdisturbanceof the right hand for objects inthe
left upper quadrant visual field.
WAB administered seven days after onset showed
severe agraphia, characterized by impaired character

104 Y. Sakurai et al. / Parietal dysgraphia
recall of both kanjiand kana, poor graphemeformation
and abnormal stroke sequences (Table 1). The patient
wrote characters slowly and laboriously. He could not
recognize orally spelled kanji characters or spell aloud
auditorily presented kanji characters, which resulted in
a low score for reading. He showed literal paragraphia
and impaired recall even for dictated single-kana char-
acters. However, the patientcouldtypekanawordsthat
he could not write in response to dictation. He copied
sentencesperfectly,buthewrote strokebystroke,refer-
ring to the sample. Most written characters were poor-
ly shaped, like geometrical figures, as if they had been
written by a child. Copying of line drawings (e.g. a
cube) was also good, but spontaneousdrawing without
a sample was done out of perspective,suggesting he al-
so had impaired mental imagery for non-linguistic fig-
ures. The visually guided reaching disturbance disap-
peared 15 days after onset but agraphia persisted even
one year post-onset.
MRI three days after onset revealed a high intensity
areawithamarginallowintensityin theleftcuneus,lin-
gual gyrus and forcepsmajor in the occipital lobe, sug-
gestingan oldhemorrhagicinfarction,and surrounding
it a thin high intensity in the left occipital and pari-
etal lobes, including the angular gyrus, precuneus and
superior parietal lobule that extended forward to the
postcentral sulcus on T2-weighted images (Figs 2–4).
2.2. Neuropsychological tests
To evaluate basic cognitive functions and language
abilities, we administered WAIS-R and WAB to each
patient (Table 1). Subtest scores of performance IQ in
WAIS-R areshownto revealcognitiveandmotorskills.
To evaluate each patient’s reading and writing ability
quantitatively, we gave them a special test (Table 2).
The task was to read aloud 100 single-character kanji
and the kana transcription of kanji characters, and to
write the same 100 dictated kanji and kana [36], all
of which are taught in the first three years of primary
school in Japan. The performances of patients 1 and 4
were recorded with a digital video camera and writing
stroke sequences were analyzed. Patient 4 was asked
to copy the test characters further.
Correct answers and time for reading and writing
were counted. In thewriting test, errors were subdivid-
ed into non-responses, partial responses (incomplete
characters or words), constructional errors (omission
or addition of a component of a character), visual er-
rors(substitution of anothervisually similar character),
phonological errors (substitution of another character
with a different phonetic value), semantic errors (sub-
stitution of another word semantically associated with
the correct word), etc. according to our previous clas-
sification [38] (Table 3). Trial and error and abnor-
mal stroke sequences were evaluated for all characters
tested. Deformity was defined as the malformation of
graphemes (characters), and was classified into dispro-
portion (imbalanced size of each component in a char-
acter or word), dislocation(wrong position or direction
of each component or stroke), line distortion (twitch-
ing of a straight line), curve distortion (twitching of
a curve), elongation of a line or stroke, and interrup-
tion of a line or stroke. Deformity was evaluated only
for correct responses. If a character had two or more
deformity types, each type was counted separately.
Whethera characteris regardedas beingwell formed
ornotdependsonanexaminer. Thus,wefirstchoseand
classified deformed characters primarily onthe basis of
the patients’ evaluation. In order to evaluate deformity
more objectively, three authors (Y.O., G.N. and T.M.),
all native Japanese, assessed the patients’ writing inde-
pendently, and a character was counted only if two or
more authors had the same evaluation of the deformity
or deformity type. Deformed characters were chosenif
twoormoreauthors’assessmentwasidenticalirrespec-
tive of the assessed deformitytype. If the order of writ-
ingstroke sequences was unusual andit was notcaused
by the patient’s writing habit, the sequences were con-
sideredto bedisordered. Impairedcharacter recall (let-
ter imagery deficit) was counted when the patient did
not make any response in writing to dictation (non-
response in Table 3). We adoptedthe followingcriteria
to diagnose apraxic agraphia: (i) production of illegi-
ble graphemes in writing that cannot be accounted for
by sensorimotor dysfunction [1,30,32], (ii) grapheme
production improves with copying [32], (iii) preserved
oral spelling or typing [32], and (iv) disorderedwriting
stroke sequences [29].
3. Results
Deformity analyses below are mainly based on the
authors’ objective assessment, if not described in par-
ticular. Patient 1 took slightly longer to write kanji and
kana, although the scores were nearly perfect. Defor-
mity involved dislocation, elongation and interruption,
and was more frequently observed in kanji (Fig. 3).
The patient took the same test four months after onset,
when he still hadparesthesia limited to the thirdto fifth
fingers and a minimal reduction in grip strength. Re-

Y. Sakurai et al. / Parietal dysgraphia 105
Table 2
Reading and writing performances of 100 single-character kanji and the kana transcription
Patient 1 2 3 4 Controls (n =11)
Mean score (SD) Mean time (SD)
Kanji reading 100 (48 s) 100 (1 min 26 s) 100
#
100 (4 min 8 s*) 99.6 (1.2) 1 min 32 s (32 s)
Kana reading 100 (1 min 28 s) 100 (1 min 13 s) 100
#
100 (2 min 27 s*) 99.6 (0.5) 1 min 13 s (24 s)
Kanji writing 99 (17 min 15 s*) 97 (23 min 2 s*) 95 (19 min*) 28* (37 min 12 s*) 95.9 (3.0) 10 min 11 s (2 min 16 s)
Kana writing 100 (12 min 10 s*) 100 (20 min 28 s*) 100 (16 min*) 50* (63 min 8 s*) 99.3 (0.9) 8 min 7 s (1 min 47 s)
Normal controls [38] were 10 men and one woman, ages 61 to 78, mean 68 years old, senior high school or university graduate volunteers who
had no past history of neurological disorders. Note that writing speed was not exactly reflected in the time spent because word-finding pauses
were also included in the time for patients 3 and 4. In patient 4, however, writing speed was obviously slow.
#
In patient 3, data for reading time were missing.
*More than 2SD above (for time) or below (for score) the normal mean.
sults showed general improvement, but he was aware
that eight kanji characters and seven kana characters
were poorly written. Patient 2 took more than twice
as long to complete the tasks as the control subjects.
Deformity consisted mainly of dislocation and elon-
gation in kanji, and curve distortion in kana, although
the patient was more aware of disproportion and line
distortion in kanji and dislocation in kana. The pa-
tient complained that he could not write characters as
he imagined, showing imbalanced kanji characters and
elongation. Although paresthesia in the third to fifth
fingers persisted, a re-examination three months after
onset showed almost perfect recovery in writing. Pa-
tient 3 spent more time writing both kanji and kana
because he wrote the wrong stroke sequences by trial
and error: He stopped writing in the middle of a kanji
character and wrote it again from the beginning, even
though the character was written correctly in six trials.
He also added a line to an incomplete kanji character
after writing it in two trials. According to the patient’s
evaluation, malformation of graphemes was more pro-
nounced in kana writing that required for curve draw-
ing [20]. Patient 4’s performance was the lowest and
he needed the longest time of the four patients. Kanji
writing was more impaired than kana writing. Most
errors were non- and partial responses resulting from
impaired recall of both kanji and kana characters, and
katakana (a form of kana that is used primarily for rep-
resenting loan words) substitution in kana. To deter-
mine the effects of visual complexity, concreteness, fa-
miliarity (how often a person has seen or used a word)
and frequency of writing single-character kanji, we di-
vided test characters into two groups (above or under
a median) nearly equal in number: a more complex
(more writing stroke sequences), concrete, familiar or
frequent group and a less complex, concrete, familiar
or frequentgroup accordingto our previousstudy [39].
Correct scores for two groups each were significantly
different in complexity (p =0.007 by Fisher’s exact
method) and familiarity (p =0.026 by Fisher’s ex-
act method), i.e. less complex and more familiar char-
acters were written more easily. The patient uttered
a word repeatedly when he had difficulty writing the
word (phonological facilitation [35]). There were a
few traces of trial and error written on a piece of paper
in kanji, but in fact the patient did many rehearsals,
moving the pencil over the paper before writing down
a character. Disordered stroke sequences were more
evident in kanji writing, when the patient appeared to
forgetthe stroke sequences of some kanji. Deformities
included dislocation in both kanji and kana and curve
distortion in kana. Copying of the 100 kanji characters
improvedoverallgrapheme formation (He thoughtthat
nineof 11 deformedcharactersin writingin responseto
dictation were written better when copying), but there
were still abnormal graphemes. He also wrote strokes
asif he had drawngeometricalfigures(abnormalstroke
sequencesincopyingkanji: 22/100). A re-examination
eight months after onset showedconsiderable recovery
(score and time: kanji 38/100 and 38 min, kana 69/100
and 44 min), but the patient still wrote poorly formed
characters with disordered stroke sequences.
Table 4 summarizes the writing features and other
clinical profiles for our four patients and reported pa-
tients with Japanese parietal agraphia [14,18,21,23,29,
45]. It is noteworthy that performance IQ was equal to
or less than verbal IQ in WAIS-R for all patients. In
patients 3 and 4 with a superior parietal lobule insult,
Block Design and Object Assembly were performed
particularly poorly. Thus, lower performance IQ prob-
ably reflects visuospatial cognitive dysfunction of the
“left” superior parietal lobule. Figure 4 shows the in-
dividual lesions of patients in Table 4 with abnormal
charactershapeformation(ourpatients 1–4)[14,21,23,
29] disordered writing stroke sequences (our patients
3,4) [14,18,23,29] and character imagery deficits (our
patients 3,4) [14,18,21,23,45] mapped onto an axial
plane through the intraparietal sulcus [8]. Lesion sites

106 Y. Sakurai et al. / Parietal dysgraphia
Table 3
Types of writing error in 100 single-character kanji and the kana transcription
Patient 1 2 3 4
Kanji total errors 1 3 5 72
Non-response 0 2 1 51
Partial response* 0 0 1 9
Constructional* 0 0 0 8
a
Neologism 0 1 2 2
Visual* 1 0 1 0
Unrelated* 0 0 0 2
Trial and error
#
0 1 15 1
Abnormal stroke sequences
#
0049
Deformity total
#
15 (28) 33 (16) 3 (5) 11 (5)
Disproportion 1 (0) 5 (0) 0 (0) 0 (0)
Dislocation 5 (10) 6 (4) 2 (1) 10 (3)
Line distortion 2 (1) 11 (1) 1 (1) 0 (0)
Curve distortion 0 (0) 3 (0) 0 (0) 1 (0)
Elongation 4 (7) 8 (3) 0 (1) 0 (0)
Interruption 3 (1) 0 (0) 0 (0) 0 (0)
Kana total errors 0 0 0 50
Non-response 0 0 0 8
Partial response** 0 0 0 21
Constructional** 0 0 0 6
b
Phonological** 0 0 0 3
Phonological and visual** 0 0 0 2
Katakana substitution** 0 0 0 10
Trial and error
#
0 0 15 10
Abnormal stroke sequences
#
0021
Deformity total
#
4 (22) 17 (12) 12 (5) 6 (6)
Disproportion 0 (1) 0 (0) 0 (0) 0 (0)
Dislocation 2 (4) 9 (0) 2 (1) 2 (2)
Line distortion 0 (0) 1 (2) 1 (0) 0 (0)
Curve distortion 2 (6) 5 (6) 8 (2) 4 (2)
Elongation 0 (3) 2 (1) 0 (0) 0 (0)
Interruption 0 (1) 0 (0) 1 (0) 0 (0)
Data were based on the results of the kanji and kana writing test (Table 2).
*Partial response: a component of a kanji character is correct. Constructional response: omission or addition of a component of a kanji
character. Visual errors: substitution of another visually similar character, e.g.
([midori], green) → ([en], margin). Unrelated
response: substitution of another kanji that has no visual or phonological similarity to the correct answer, e.g.
([natsu], summer) →
([susumeru], recommend).
**Partial response: one character or more in a kana word is correct. Constructional response: omission or addition of a component of a
kana. Phonological response: one or more characters of a kana word were substituted for other kana (phonemic paragraphia), e.g.
([shiru], know) → ([hiru], noon). Phonological and visual response: changing one character into another visually similar to the
target character, e.g.
([kuroi], black) → ([kurui]). Katakana substitution: substitution of Katakana (a form of kana that is
used primarily for representing loan words) that has the same phonemic value, e.g.
([kuruma], wheel) → ([kuruma]).
a
Constructional errors consisted of five deletions of one stroke and three interruptions of one stroke.
b
Constructional errors consisted of five deletions and one addition.
#Trial and error and abnormal stroke sequences were evaluated for all characters tested. Trial and error denotes an attempt to write
an incorrect or incomplete character repeatedly. Deformity was evaluated only for correct responses. Scores denote the patient’s
subjective evaluation and three authors’ assessment (in the parentheses). In the three authors’ assessment, a character was counted only
if two or more authors had the same evaluation of the deformity or deformity type. Deformed characters were chosen by two or more
authors’ evaluation whether or not the deformity type assessment was identical among authors. Eventually, the number of deformity
total exceeded the sum of each deformity type in all patients. If a character had two different deformity types, these two were counted
separately. Disproportion refers to the imbalanced size of each component in a character or word. Dislocation is the wrong position
or direction of each stroke. Distortion is the twitching of a straight line or curve. Elongation and interruption are of a line or stroke.
were delineated with a sheet of lettering screen and
each lesion image cutout was overlapped on the stan-
dard axial plane at the level of the intraparietal sulcus.
All three symptoms involved lesions surrounding the
intraparietal sulcus (overlapped area). In particular,
the overlapping appears more pronounced in the ante-
rior half of the intraparietal area in disordered stroke
sequences (middle), and extensive areas including the
supramarginal gyrus or the precuneus in character im-
agery deficits (right side).

Y. Sakurai et al. / Parietal dysgraphia 107
Fig. 3. Examples of abnormal grapheme formation and disordered writing stroke sequences in patients 1 to 4. Number corresponds to the patient
number. An arrow head denotes the part of deformity. All samples of the deformity type were based on three authors’ objective assessment. In
patients 3 and 4, stroke sequence errors were frequently accompanied by trial and error, as in patient 3 (orthodox stroke sequences are shown on
the right). Patients 1, 2 and 4 underwent the same test in a follow-up study. Abbreviations. 3M: three months after onset, stroke: stroke sequence
disorder.
4. Neuroimaging study
All four patients underwent SPECT with the
99m
Tc-
ethylcysteinate dimer (ECD-SPECT) 17 days (patient
1), 21 days (patient 2), 33 days (patient 3) and 21
days (patient 4) after onset. SPECT data were trans-
formed into the Analyze Format and were normalized,
smoothedandcorrectedforinter-laboratorydifferences
with a 3-dimensional conversion map [24]. For this
system,realignment,spatialnormalizationandsmooth-
ing are essentially the same as thoseof Statistical Para-
metric Mapping (SPM) Version 1999, and the statisti-
cal significance was determined with SPM 96 for Win-
dows. Thedatawerecomparedwiththoseofthenormal
subject database of the same generationat the National
Center of Neurology and Psychiatry, Tokyo (n =20).
Areas showing a significant decrease in cerebral blood
flow (corrected p<0.01) were rendered on standard
brain surface images (Fig. 5). Reduced blood flow was
found in the postcentral gyrus in all four patients. In
addition, the precentral gyrus was affected in patient
1 with the left hand weakness and limb apraxia. The
superior parietal lobule was involved in patients 1, 3
and 4, the angular gyrus in all patients, and the supra-
marginal gyrus in patients 1 and 3.

108 Y. Sakurai et al. / Parietal dysgraphia
Table 4
Summary of the reported cases of Japanese parietal agraphia and the present patients
Authors Writing Apraxia Other symptoms WAIS-R Lesion
Shape Speed Stroke Imagery Copying
Kawamura [18] Pt 1 N ? I I N – LR, FA, AC V 97, P 97 SPLa, SMG
Pt 2 N ? I I N IMA LR, FA, AC V 88, P 74 SPLa, SMG
Kojima et al. [21] Pt 1 I ? N I I IA CD, USN, TD V 98, P 68 SPLp, Cu, Sup O
Ishiai et al. [14] Pt 2 I I I I I – – V 107 SPLap
Toyokura et al. [45] N ? N I N – – not done sSPLap, sAG, Cu
Maeshima et al. [23] I I I I I – – V 94, P68 SPLap, AG
Otsuki et al. [29] I ? I N I – – V 109, P 100 SPLa
Our Pt 1 I I N N sl. I LA TA V 89, P 73 Post C, SMG
Pt 2 I I N N sl. I – TA V 107, P 94 Post C
Pt 3 sl. I N I sl. I N – FA, AC V 116, P108 SPLap, SMG
Pt 4 I I I I I – AC, RD V 94, P 65 SPLap, SMG, AG,
Cu, Sup O
The evaluation of shape (grapheme formation), speed (writing speed), stroke (writing stroke sequences) and imagery (non-response that is due
to poor character recall) in writing in response to dictation, and copying (copying the visually-presented characters) were based on the authors’
assessment described in the original papers.
Abbreviations. I, impaired; N, normal; sl., slightly; V, verbal IQ; P, performance IQ; Pt, patient; LR, left-right disorientation; FA, finger
agnosia; IA, ideational apraxia; IMA, ideomotor apraxia; LA, limb apraxia; CD, constructional disorder; USN, unilateral spatial neglect; TD,
topographical disorientation; AC, acalculia; RD, visually guided reaching disturbance; SPL, superior parietal lobule; a, lesion extending anteriorly
to the postcentral sulcus; p, lesion extending posteriorly to the parieto-occipital junction; ap, lesion extending both anteriorly and posteriorly;
s, sub-cortical; AG, angular gyrus; Cu, cuneus and precuneus; Sup O, superior occipital gyrus; SMG, supramarginal gyrus; Post C, postcentral
gyrus.
Fig. 4. Overlapped lesions in the parietal lobe in patients with abnormal character shape formation, disordered writing stroke sequences and
character imagery deficits (impaired character recall). An arrow head denotes the central sulcus. The axial image through the intraparietal sulcus
was drawn from Damasio [8]. All three symptoms involved lesions surrounding the intraparietal sulcus. The overlapping was more pronounced
in the anterior half of the intraparietal area in disordered stroke sequences (middle), and extensive areas in the parietal lobe in character imagery
deficits (right side).
5. Discussion
The four patients reported here all exhibited writing
impairments from parietal lobe lesions. Patient 1 was
left-handed. As his impairment, however, was solely
caused by damage to the sensorimotor area, the discus-
sion could be applied to right-handers. In addition, a
slightlyshorteneddigitspanforhisage(thispatienthad
a small infarction in the supramarginal gyrus) suggests
that patient 1’s language functionwas performed in the
right hemisphere. Patient 3 had a bilateral lacunar in-
farctioninthecentrumsemiovale,butthisoldinfarction
had little effect on the patient’s general cognitive func-
tion, as revealed by WAIS-R. Patient 4 had sustained
a cerebral hemorrhage in the left medial occipital gyri
and the right homonymous hemianopia had remained.
Additionalinfarctionin the adjoining area in the occip-
ital and parietal lobes produced severe agraphia with
impaired character recall. Thus, this new lesion in the
superior parietal and parieto-occipital areas was criti-
cal in the occurrence of agraphia, although his reading
and writing speed were also affected by hemianopia
(discussed in 5.4).
Since apraxic agraphia presupposes normal sensori-
motorfunction[1,32],it is clearthatpatients1and2 did
not have apraxic agraphia. Instead, they demonstrat-

Y. Sakurai et al. / Parietal dysgraphia 109
Fig. 5. Decreased blood flow in the four patients determined with SPM 96 in ECD-SPECT. Patient data were compared with those of a normal
database of the same generation in the National Center of Neurology and Psychiatry, Tokyo (n =20). A significant decrease in cerebral blood
flow was shown (corrected p<0.01). Reduced blood flow was found in the postcentral gyrus in all four patients. The superior parietal lobule
was involved in patients 1, 3 and 4. Note that the localized region of the somesthetic sensory area was affected in patients 1 and 2, who exhibited
grapheme deformity.
ed that dysgraphia, i.e. abnormal grapheme formation,
occursbecause of a postcentralgyrus lesion, regardless
of accompanyinglimb apraxia.
Patients3and4hadapraxicagraphiainthe sensethat
they showed (i) abnormal grapheme formation, (ii) im-
provement in poorly formed characters when copying,
(iii) preserved kana word typing (patient 4), and (iv)
disordered writing stroke sequences. Impaired char-
acter/letter recall (letter imagery deficit) is sometimes
observedin apraxic agraphia [7,22]. Evenif thepatient
does not spell aloud completely a word that he cannot
write, this does not exclude the diagnosis of apraxic
agraphia. Recognitionoforallyspelledkanjicharacters
andoralspellingofkanjicharacterswerepoorinpatient
4(Table1),suggestingkanjicharacterimagerydeficits.
Recognition of orally spelled kanji characters was also
poor in patient 3. In addition, the fact that he wrote
a character again from the beginning, even though the
character was written correctly, suggests that the visual
image of the character was unstable. In short, patient
3 had slightly, and patient 4 severely, impaired mental
imagery of kanji. We discuss the anatomical substrates
of mental imagery deficits in 5.3.
According to a cognitive neuropsychological
model [10,30], the writing process can be subdivid-
ed into central (or linguistic) and peripheral (or mo-
tor) components. Central components are responsi-
ble for selecting the appropriate words for written out-
put,whereasperipheralcomponentsare responsiblefor
converting orthographic information into handwriting
movements. We prefer the terminology of linguistic
vs. motor to that of central vs. peripheral because all
these processes occur in the “central” nervous system.
From this point of view, all four patients had motor
impairmentsof handwriting, and in addition, patients 3
and 4 had linguistic disorders of word/character recall.
5.1. Abnormal grapheme formation
Patients1and2showedthat charactershape wasdis-
turbed with a postcentral gyrus lesion, with or without
limb apraxia. Abnormal grapheme formation due to a
postcentralgyruslesion has notbeenreportedprevious-
ly. It is clear that the deficit lay in the motor aspect of
handwriting. However,thesecasesarenotdelineatedin

110 Y. Sakurai et al. / Parietal dysgraphia
thecognitiveneuropsychologicalmodelofspellingand
writing [10,30,32]. It is likely that sensory and kines-
thetic feedback from the writing hand ascended to the
opposite somesthetic sensory or somatosensory hand
area (Areas 1,2 and 3), but the partial damage had an
inappropriateeffecton themotorprogramming[32](or
graphic innervatory patterns [30], anatomically Area 4
handarea)or directlyinfluencedthe corticospinal tract.
It is known that descending fibers from the postcentral
gyrus (Areas 1, 2, and 3) join the corticospinal tract
from the precentral gyrus (Area 4) [34]. Functional
neuroimaging studies also suggested the involvement
of the postcentral gyrus in handwriting [4,16]. Thus,
we designate this type of writing impairment “somes-
thetic dysgraphia.”
It is difficult to differentiate the character deformity
in patients 1 and 2 from that in patients 3 and 4 with
apraxic agraphia. Analysis of writing errors, however,
showed that in kanji writing dislocation accounted for
many errors in patients 3 and 4, whereas there were
many elongation errors other than dislocation in pa-
tients 1 and 2 (Table 3). This difference is probably
because acquired information about spatial alignment
ofeach componentor stroke was disturbedin patients 3
and4(describedin5.6),whereas the deficit waslimited
to fine control of handwriting in patients 1 and 2.
Regarding the neural substrate, our patient 3 and
reported cases [14,21,23,29] suggest that abnormal
grapheme formation arises from lesions surrounding
the intraparietal sulcus (Fig. 4, left side). In addition,
graphemic distortion seems to be more pronounced
when the parietal lobe lesion extends to the superior
occipital gyrus and precuneus, as in our patient 4.
5.2. Writing stroke sequence disorder
Disordered writing stroke sequences are another
symptom that characterizes apraxic agraphia. This
symptom is easily observed, especially in writing of
kanji that have multiple stroke sequences [29], but it
has also been reported in Western countries [6], where
a video camerawas used. Reported patients [14,18,23,
29] and our patients 3 and 4 suggest that a lesion in
the intraparietal area, particularly the anterior part that
extends forward as far as the postcentral sulcus, caus-
es abnormal writing stroke sequences (Fig. 4, middle).
Thus, an area adjoining the postcentral gyrus in the in-
traparietal sulcus seems to be critical to the occurrence
of disordered writing stroke sequences.
5.3. Mental imagery deficit of kanji and kana
We can see in Fig. 4 (right side) that letter/character
imagery deficits (impaired character recall) were also
attributed to the damage surrounding the intraparietal
sulcus, but in some cases the lesion extended inferi-
orly to the supramarginal and angular gyri [18,23,45]
or posteriorly to the superior occipital gyrus and pre-
cuneus [21,45]. The involvement of the inferior pari-
etal and posterior occipital gyri was also observed in
reports from Western countries [7,22], in which mental
imagery of letters was impaired. Comparison of the
symptom-to-lesion between patients 3 and 4 suggests
that mental imagery is pooreras the lesion involves the
angular, superior occipital and precuneus gyri.
In patient 4, impaired character recall was more
prominent in kanji, but kana character recall was also
disturbed,whichwasnotobservedin patients 1, 2and3
(Tables1and2). Reportedcases showedagraphiamore
impairedforkanji[14,17,23]andagraphiaforbothkan-
jiandkana[17,21,29,45]witha superiorparietallobule
lesion. This difference probably depends on whether
the lesion extendsinferiorlyto the supramarginalgyrus
or angular gyrus, or posteriorly to the parieto-occipital
junction. A lesion in the posterior area of the superi-
or parietal lobule alone or around the intraparietal sul-
cus can yieldagraphia more impairedfor kanji [14,17].
Furthermore, it is often seen that agraphia that impairs
kana writing morethan kanji writing occurs becauseof
asupramarginalgyruslesion[37,43],whereasagraphia
that impairs kanji writing more than kana writing oc-
curs because of an angular gyrus lesion [14,15,17,25,
38]. Since the inferior supramarginal gyrus is thought
to be the phonological short-term-memory store [37]
and kana characters directly represent a sequence of
phonemes (consonant-vowel syllables), it is quite un-
derstandable that agraphia or literal paragraphia for
kana occurs due to damage to the supramarginalgyrus.
In this case, however, it should be noted that most of
the errors were not impaired recall, but literal para-
graphia[35,43]. Patient1withthesupramarginalgyrus
damagedidnotexhibita phonologicalshort-termmem-
ory impairment or kana agraphia. This is probably be-
cause the lesion was too small to produce symptoms
(strictly speaking, his digit span forward 6 was slightly
low for his age, as described). Hypoperfusion of the
parietal lobe in the patient’s SPECT image probably
reflected relative ischemia caused by occlusion of the
right middle cerebral artery.
Conversely, it is not clear why kanji writing is more
disturbed than kana writing in an angular gyrus lesion.

Y. Sakurai et al. / Parietal dysgraphia 111
We believe that orthographicinformationfrom the pos-
terior inferior temporal cortex is sent by way of the an-
gular gyrus (probably through the subcortical associa-
tionfibers)to thesuperiorparietallobule,andthis route
is interrupted by damage to the angular gyrus, which
produceskanji orthographyrecall deficits [35] (Fig. 6).
Kana writing is also disturbed in an angular gyrus le-
sion, although there are few errors [14,15,17,25,38]. In
our study [38], errors included phonological and con-
structional (omission or addition of a component of a
kana character) errors.
Thelesionextensiontotheparieto-occipitaljunction,
i.e. the superior occipital and precuneus gyri, is prob-
ably another factor that influences the kanji vs. kana
difference. As patient 4’s kana writing errors consisted
mostly of non- and partial responses (impaired recall)
with a few phonological errors (literal paragraphia), it
is clear that they were not attributable to dysfunction
of the supramarginal gyrus or angular gyrus. Instead,
the superior parietal lobule and the adjoining superior
occipital and precuneus gyri seem to be concerned in
recalling kana, as well as kanji, orthography. Damage
to this area may give rise to imagery deficits of both
kanji and kana (graphemic area in a broad sense, dis-
cussed in 5.6), but kanji are more affected because of
their complex configuration. In support of this view,
a visual complexity effect (less complex characters are
recalled and written better than more complex charac-
ters) was observed in patient 4’s performance in the
100 kanji writing test.
In summary, mental imagery may be more serious-
ly affected as the lesion extends from the intrapari-
etal area to the angular, superior occipital and pre-
cuneus gyri. Furthermore, the involvement of the
supramarginal gyrus, angular gyrus or superior occip-
ital and precuneus gyri can determine the severity of
kanji or kana recall impairment. A lesion restricted to
the anterior area of the superior parietal lobule may not
cause a character recall impairment [29].
5.4. Reduced writing speed
Writing speed was obviously low for patient 1. Re-
duced writing speed was probably caused by weakness
of the damaged hand or insufficient sensory and kines-
thetic feedback from the damaged hand during writing
becausetheWAIS-RDigitSymbolsubtestperformance
was also poor in patient 1 (Table 1). Although patient
2 got a normal score compared with normal controls
in the Digit Symbol subtest, the fact that his time for
writing in the 100-kana writing test (mental imagery
Fig. 6. Diagram of an anatomically based dual-route hypothesis for
writing in response to dictation (modified from Sakurai et al. [35]).
a. phonological pathway, b. orthographic pathway, c. interaction
between phonology and orthography, d. interaction between parietal
graphemic area and frontal hand area. Phonological information of
a word goes from the primary auditory cortex (Heschl’s gyri) and
the posterior superior temporal gyrus (Wernicke’s area) to the angu-
lar and supramarginal gyri and joins the arcuate fasciculus to travel
to the frontal motor and premotor areas (a, phonological route). A
phoneme-linked visual image of kana or a syllable is accessed in the
angular gyrus and the adjoining lateral occipital gyri and then the
visual information of kana joins the orthographic route to travel to
the frontal cortex. The posterior superior temporal gyrus (P), where
the phonological information of words is stored, and the posterior
inferior temporal cortex (O; Brodmann Area 37), where the ortho-
graphic information of words is stored, have a reciprocal connection
(c). Lexico-semantic information (S) is stored in extensive areas in
the left temporal lobe, and can be accessed either through the poste-
rior superior temporal gyrus during listening or through the posterior
inferior temporal cortex during reading (illustrated in dotted lines).
Orthographic information (visual images of kanji words and charac-
ters and also kana words) goes from the posterior inferior temporal
cortex and proceeds upward under the angular gyrus and the superior
parietal lobule to travel to the premotor hand area (H; Areas 44/45
and 6). This orthographic route (b) goes directly or indirectly to the
hand area via the parietal graphemic area (G) where visuokinesthetic
and sequential motor engrams for letters and words are stored. The
graphemic area in a broad sense includes the inferior parietal lob-
ule and parieto-occipital junction (superior occipital and precuneus
gyri), in addition to the superior parietal lobule and intraparietal area,
and stores visuospatial attributes of characters. Kanji characters that
are graphically complex and have multiple stroke sequences depend
more on the orthographic route, whereas kana characters that link
directly to phonemes and have a graphically simple configuration
depend less on the orthographic route. The parietal graphemic area
and the frontal hand area (H) have a reciprocal connection (d).
is less involved in this test) recovered three months
later (from 20 to 14 min) suggests that patient 2 also
had a low writing speed at disease onset solely because
of insufficient sensory and kinesthetic feedback. Con-
versely, Patient 4 was extraordinarily slow at writing.
One reason is that he had right hemianopia. Another
reason is probably associated with the poor grapheme
formationin apraxicagraphia. That is, because of a de-
fective visuokinesthetic engram (sequential motor pat-

112 Y. Sakurai et al. / Parietal dysgraphia
terns)for words and letters, ormoregenerallysymbols,
the patient could not write or spell words properly and
smoothly, and this required a lot of time. Patients with
apraxic agraphia who had a low writing speed as well
as poor grapheme formation have been reported [14,
23].
5.5. Neuroimaging data
The SPECT data showed extensive areas of hypop-
erfusion in the temporo-parietal and parieto-occipital
junctions in all patients (Fig. 5). For patient 1, oc-
clusion of the right middle cerebral artery was asso-
ciated with the hypoperfusion of these areas. For pa-
tients 2 and 3, left-side dominant enlargement of the
lateral ventricles seemed to influence the blood flow of
the temporo-parietal junction. As patients 1 and 2 did
not show other cognitive impairment except for motor
dysgraphia, hypoperfusionof the temporo-parietal and
parieto-occipital areas is irrelevant to the symptoms.
Blood flow reduction in thelocalized area of the senso-
rimotor cortex in patient 1 and the somesthetic sensory
area in patient 2 supports our view that these areas are
also involved in grapheme formation. Patient 3 had
minimal impairment of character recall (letter imagery
deficit). It is possible that decreased blood flow to the
supramarginaland angulargyri had some effect on per-
formance. Even so, however, this does not alter the
conclusionthat more extensive areas in the parietal and
occipital lobes are needed to cause severe deficits of
graphemeformationandmentalimagery,whichisclear
from the comparison of blood flow images between
patients 3 and 4.
Functional imaging studies have revealed activation
of the posterior inferior temporal cortex, intraparietal
area, superiorparietal lobule,sensorimotorcortex,pos-
terior middle frontal gyrus, dorsolateral prefrontal cor-
tex, and supplementary motor area in a variety of writ-
ing tasks [4,16,26,27,44]. These activated areas in-
clude all the lesion sites of our patients. Among them,
the posterior inferior temporal cortex and intraparietal
area were also activated in mental recall of kanji and
kana characters [26,27], suggesting that they were en-
gagedin retrievalof orthography. Besides, the superior
parietal lobule, sensorimotor cortex, posterior middle
frontal gyrus and supplementary motor area were acti-
vated while writing in contrast to naming [4], suggest-
ing that they were concerned with the motor aspect of
handwriting. It should be noted that the superior pari-
etal lobule or intraparietal area was activated during
both word recall and handwriting, which implies that
theintraparietalarea plays an importantrolein wordre-
call, orthography-to-motor transcoding and execution
of handwriting movements.
5.6. Modified dual-route hypothesis for writing
To account for abnormal letter formation and let-
ter imagery deficits (impaired letter recall) in apraxic
agraphia, a graphemic area responsible for transcod-
ing features of letters into graphemic production pat-
terns [33] was considered to regulate both motor
transcoding of letter features and letter imagery [7].
Apraxic agraphia was assumed to result from a disrup-
tion of the parietal graphemic area or disconnection of
output from the graphemic area [32]. Another theo-
ry attributes the function of motor transcoding to the
graphic motor programs that specify the sequence, di-
rection and relative size of strokes [9,30]. It remains
unclear whether grapheme formation and mental im-
agery are performed in an anatomically identical area.
Our patients 3 and 4 suggest that the intraparietal area
is crucial for both letter formation and letter imagery,
butmore extensiveareas in the inferior parietal, superi-
or occipital and precuneus gyri are involvedin a severe
deficit of letter imagery (letter recall). Also, in the in-
traparietal area, the anterior part seems to be more con-
cerned with writing stroke sequences (described earli-
er).
Given these findings, we can now modify the dual-
route hypothesis for writing that we described in In-
troduction. That is, the graphemic area (or graphic
motor programs) in a narrow sense is located in the
anterior intraparietal area posterior to the postcentral
gyrus, stores visuokinesthetic [32] or sequential motor
engrams for words and letters linked to handwriting,
andsends this informationto the frontal motorand pre-
motor areas (hand area) (H in Fig. 6). The premotor
hand area is located in the posterior middle and infe-
rior frontal gyri (Areas 44/45 and 6), receives phono-
logical, orthographic and visuokinesthetic information
about words and letters from the posterior area, and
links these three sources of information to send them
to the motorarea (Area 4) to execute handwriting. The
orthographic route (b in Fig. 6) goes directly or indi-
rectlyvia the parietalgraphemicarea (G in Fig. 6)tothe
frontalhand area. The directorthographicrouteis used
when a person recalls the visual image of a character,
whereasthe indirectorthographicrouteis usedwhenhe
writes a character in response to dictation. The parietal
graphemic area and frontal hand area have a reciprocal
connection. As we write a word or letter repeatedly,

Y. Sakurai et al. / Parietal dysgraphia 113
visuokinesthetic and sequential motor information for
wordsand letters is sent backfromthefrontalhandarea
to the parietal graphemic area, connects to the visual
images from the orthographic route, and is stored there
as an engram. This visuokinesthetic and sequential
motor information is in turn transmitted to the frontal
hand area when we write words spontaneously.
Patients with apraxic agraphia caused by damage to
the graphemic area (G in Fig. 6) can spell alouda word
using the direct orthographic route, but probably can-
not express the writing stroke sequence. Conversely,
in disconnection type apraxic agraphia (interruption of
outputfromG to H in Fig. 6)[29], patients not only can
spell a word aloud but also can orally state the stroke
sequence using the direct orthographic route and the
recurrent route from H to G in Fig. 6. The interaction
between the parietal graphemic area and frontal hand
area also explains why a patient with letter shape im-
agerydeficits canstillproducewell-formedletters[40].
According to the present theory, this patient had dam-
age to the orthographicroute at a point before the route
is divided into the direct and indirect pathways. More-
over, “somesthetic dysgraphia” (patients 1 and 2) re-
sults from inappropriate sensory or kinesthetic feed-
back to the frontal hand area from the damaged post-
central somatosensory hand area.
Thishypothesispredictsthatapraxicagraphiacaused
by a lesion restricted to the anterior intraparietal area
does not produce letter imagery deficits (impaired let-
ter/character recall). This is because visual images of
wordsand letters aretransmittedthroughthe intact sub-
cortical association fibers via the direct orthographic
routein the parietallobe, althoughit is possiblethat the
direct orthographic route is somewhat affected by the
cortical damage. Unstable visual images of characters
(patient3)probablyreflectthis modulationeffectof the
deficient parietal cortexon the orthographicrouteor on
the frontal hand area.
In addition, grapheme formation and letter recall are
more disrupted when a lesion involves the posterior in-
traparietal, inferior parietal, superior occipital and pre-
cuneus gyri (patient 4). It is assumed that visuospatial
attributes of a character (i.e. spatial alignment of each
stroke) linked to handwriting are processed and stored
there (graphemic area in a broad sense). As a result,
kanji characters that have a complexconfigurationmay
bemoredeformedanddifficultto recall than kanachar-
acters with this extensive lesion. Regarding this point,
it should be noted again that activation of the superi-
or parietal lobule and intraparietal area in both writing
and mental recall was more widespread in kanji than in
kana [26].
We should draw attention to the fact that let-
ter/character imagery deficits (impaired character re-
call) do not solelyoccur because ofdamage to the pari-
etalgraphemicarea,butalsoduetodamagetotheangu-
lar gyrus [14,15,17,25,38] and posterior inferior tem-
poralcortex[19,36,41]. Ourhypothesiscanaccountfor
letter/character imagery deficits from different lesion
sites, which are difficult to explain using the previous
hypotheses.
As the present argument is based on only a few pa-
tients, further case studies are required to determinethe
anatomical substrates of grapheme deformity, writing
stroke disorder and imagery deficits and also the role
of the superior parietal lobule in writing.
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