Neurocase
The Neural Basis of Cognition

ISSN: 1355-4794 (Print) 1465-3656 (Online) Journal homepage: http://www.tandfonline.com/loi/nncs20

Unilateral Apraxic Agraphia without Ideomotor
Apraxia from a callosal lesion in a patient with
Marchiafava-Bignami disease
T. Kesayan & K.M. Heilman
To cite this article: T. Kesayan & K.M. Heilman (2018): Unilateral Apraxic Agraphia without
Ideomotor Apraxia from a callosal lesion in a patient with Marchiafava-Bignami disease, Neurocase,
DOI: 10.1080/13554794.2018.1444780
To link to this article: https://doi.org/10.1080/13554794.2018.1444780

Published online: 26 Feb 2018.

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NEUROCASE, 2018
https://doi.org/10.1080/13554794.2018.1444780

Unilateral Apraxic Agraphia without Ideomotor Apraxia from a callosal lesion in a
patient with Marchiafava-Bignami disease
T. Kesayana,b and K.M. Heilmanc,d
a
Department of Neurology, University of South Florida Morsani College of Medicine, Tampa, FL, USA; bDepartment of Neurology, James A. Haley
Veteran’s Affairs Hospital, Tampa, FL, USA; cNeurology Service and GRECC, Malcom Randall Veterans Affairs Medical Center, Gainesville, FL, USA;
d
Department of Neurology, University of Florida College of Medicine, Gainesville, FL, USA

ABSTRACT

ARTICLE HISTORY

Apraxic agraphia can be caused by left hemispheric cerebral lesions in the area that contains the spatial
representations of the movements required to write, from a lesion in, or connections to, the frontal
premotor cortex that converts these spatial representations to motor programs (Exner’s area). A righthanded woman with Marchiafava Bignami disease and lesions of the genu and splenium of her corpus
callosum had apraxic agraphia without ideomotor apraxia of her left. A disconnection of Exner’s area in
the left hemisphere from the right hemisphere’s premotor and motor areas may have led to her
inability to write with her left hand.

Received 2 December 2017
Accepted 19 February 2018

Introduction
Marchiafava-Bignami (MB) disease was first described in 1903
as a rare and fatal disease in Italians who heavily drank wine
(Marchiafava & Bignami, 1903). MB disease is characterized by
demyelination and later necrosis of the corpus callosum seen
mainly in people who are alcoholics, but is also very rarely
seen in other conditions, such as diabetes mellitus (Lakatos
et al., 2014). Patients with MB typically present with cognitive
impairments, hypertonia, gait abnormalities, and dysarthria,
and some may develop seizures (Heinrich, Runge, & Khaw,
2004). Recently, Heinrich and colleagues categorized patients
with MB into two types (Heinrich et al., 2004). Type A often
presents with coma or stupor and is often associated with
disability, with about a 21% death rate. In contrast, Type B is
less commonly associated with disability, and patients with
this disorder rarely die. These two subtypes often also differ in
the forms of damage to the corpus callosum. Whereas the
patients with Type A have most of their corpus callosum
damaged, those with Type B often have focal corpus callosum
injury, the most common areas being the splenium and the
genu (Delangre et al., 1986).
An inability to perform skilled and purposeful actions in the
absence of weakness, sensory loss, movement disorders, or any
other confounding medical complications limiting fine motor
movements is termed apraxia. The term apraxia was first used
by Steinthal to describe an inability to correctly perform purposeful movements in the absence of weakness (Steinthal, 1871).
Although Steinthal is credited for the term, it was Hugo
Liepmann who made many of the first major contributions to
the understanding of apraxia. In a series of papers, (Liepmann,
1905, 1920; Liepmann & Maas, 1907), Liepmann described ideomotor apraxia (IMA) where patients often make postural errors
such as using body part as a tool (Goodglass & Kaplan, 1963) as
well as making incorrect movements of their joints in relation to
CONTACT T. Kesayan

tkesayan@health.usf.edu

© 2018 Informa UK Limited, trading as Taylor & Francis Group

KEYWORDS

Agraphia; Apraxia;
callosal disconnection;
Marchiafava- Bignami

their body and in relation to objects with which they are interacting (Poizner, Mack, Verfaellie, Rothi, & Heilman, 1990; Rothi,
Mack, Verfaellie, Brown, & Heilman, 1988). Liepmann and Maas
(1907) described a patient with a lesion of the corpus callosum
who revealed an IMA of his left upper limb; however, this patient
had a prior right hemiparesis from a pontine lesion as well as a
medial left frontal lesion. As medial left frontal injury may produce an IMA of both hands and this patient’s right hand could
not be tested, it is not clear if this patient had a unilateral callosal
ideomotor apraxia (Watson, Fleet, Gonzalez-Rothi, & Heilman,
1986). However, subsequently, unilateral left upper limb IMA
induced by a callosal lesion has been reported (Graff-Radford,
Welsh, & Godersky, 1987; Watson & Heilman, 1983).
Patients with limb kinetic apraxia (LKA), as described by
Liepmann (1920), have a loss of deftness with an impaired
ability to make independent and precise coordinated movements with their hand and fingers. Kleist also described
patients with a similar disorder that he called “innovatory
apraxia.” (Heilman & Watson, 2008; Kleist, 1934). Verstichel
and Meyrignac described a patient with an infarct involving
the anterior and middle parts of the corpus callosum who had
an impairment in the ability to make fast and deft movements
with his left hand (Verstichel & Meyrignac, 2000). Acosta,
Bennett, and Heilman also described a patient with a lesion
in the body of the corpus callosum who had an IMA, as well as
LKA of his left hand, when tested with the coin rotation test
(Acosta, Bennett, & Heilman, 2014).
Apraxic agraphia is a disorder where a person is impaired in
making the finger, hand, and arm movements needed to correctly
write in the absence of primary sensorimotor disorders as well as
without impaired language, spelling, or typing abilities (Heilman,
Coyle, Gonyea, & Geschwind, 1973; Heilman, Gonyea, &
Geschwind, 1974; Heilman & Watson, 2008; Valenstein &
Heilman, 1979). Patients have been described who have apraxic

2

T. KESAYAN AND K. M. HEILMAN

agraphia without other forms of limb apraxia. For example,
Roeltgen and Heilman (1983) described a 75-year old righthanded man with a right parietal lesion who demonstrated agraphia with preserved spelling, and was without any form of limb
apraxia (Roeltgen & Heilman, 1983). These authors suggested that
this right-handed man with crossed aphasia had apraxic agraphia
because the movement representations for writing were located
in the damaged right hemisphere, but his non-damaged left
hemisphere was mediating the movement representations for
other forms of purposeful movements. Coslett and colleagues
described two right-handed patients with left hemisphere language dominance who suffered from left middle cerebral artery
(MCA) territory infarcts in whom praxis and writing were affected
differently (Coslett, Gonzales Rothi, Valenstein, & Heilman, 1986).
One patient had apraxic agraphia without language impairments
or other types of limb apraxia; whereas, the other patient had
linguistic agraphia and an ideomotor apraxia, with no impairment
in grapheme production (1986). These authors suggested that like
the dissociation between linguistic and motoric components of
writing (1986), these cases illustrate that IMA and apraxic agraphia
can be dissociated and therefore are separate entities.
The reports demonstrate that apraxic agraphia can occur in
the absence of other forms of limb apraxia, aphasia, or linguistic
agraphia. This dissociation suggests that different movement
representations are essential for writing and for performing
other transitive and intransitive movements of the upper limb
and that these two different types of movement representations
are stored in different parts of the brain (Coslett et al., 1986;
Heilman & Watson, 2008; Roeltgen & Heilman, 1983). There
have also been reports of patients with apraxic agraphia from
callosal lesions (Falchook, Watson, & Heilman, 2016; Liepmann &
Maas, 1907; Watson & Heilman, 1983); however, these patients
also had IMA. In addition, there have been reports of patients
with callosal lesions who revealed left upper limb IMA and LKA,
but without apraxic agraphia (Acosta et al., 2014). These reports
of dissociation between the hemispheric and callosal lesions that
induce an IMA or LKA, without an apraxic agraphia, and vice
versa, provide support for the postulate that the graphemic
movement representations are stored in different areas than
those that store other transitive and intransitive movement
representations. In addition, these graphemic movement representations are also transferred across the corpus callosum in a
different area than the one that transfers other movement representations. To the best of our knowledge, however, there has

been no report of a patient with unilateral (left-handed) apraxic
agraphia in the absence of an IMA. In addition, we are unaware of
any reports of patients with MB who revealed a unilateral apraxic
agraphia.

Case report
Our patient is a 38-year-old right-handed Caucasian woman
with 1 year of declining cognition and a 2-week history of
difficulty with speech and inability to walk prior to hospitalization. Over the past year, she has had a progressive decrease in
her appetite. She had worked as a propane delivery truck
driver up until 3 weeks prior to presentation.
On her initial physical examination, she was awake, agitated, could intermittently follow simple commands, had a
spastic dysarthria, and was only able to say several words.
On cranial nerve examination, her extraocular movements
were full and without nystagmus. Her pupils were round
and reactive to light and accommodation. Her face was
symmetric, and her palate elevated symmetrically. On
motor examination, she was cachectic, had a fine high
frequency tremor in both hands and all fingers with arms
outstretched, had an increased spastic tone in her limbs,
and a mild ataxia with movements of arms and legs. Her
deep tendon reflexes were 3+ and symmetrical at biceps,
brachioradialis, patella, and Achilles tendon. Initially, a sensory examination could not be adequately performed owing
to her cognitive and speech difficulties. She was also unable
to safely stand or walk.
Laboratory evaluation including a complete blood count
and comprehensive metabolic panel was within norms except
for a low albumin level of 2.6 mg/dL (normal 3.5–5.0 mg/dL).
Her vitamin B12 level was 1146 pg/mL. It was not known if she
was recently given vitamin B12 supplementation. Her vitamin
B1 level was below 7 nmol/L (8–30 nmol/L), the lowest detectible level for the testing laboratory. Analysis of the cerebrospinal fluid (CSF) revealed a colorless fluid with 4 red blood cells
(RBC), 1 nucleated cell, a protein of 37 (15–45 mg/dL), and a
glucose of 54 (40–70 mg/dL). Table 1 provides the results of
her serum and CSF laboratory evaluations.
In addition to the tests depicted in Table 1, a urine drug
screen was also conducted on the day of presentation, and
was only positive for cannabinoids. An MRI of her brain
showed restricted diffusion in the genu and splenium of

Table 1. Serum and cerebrospinal fluid (CSF) laboratory evaluations.
SERUM
Homocysteine
Vitamin B12
Folate
Methylmalonic acid
Ceruloplasmin
Vitamin B1
Vitamin B6
Vitamin D
Alpha-tocopherol
Beta-gamma tocopherol
TSH
Albumin
Calcium
Phosphorus

CSF
7.9 (nl 5.1–15.4 umol/L)
1146 (nl 189–883 pg/mL)
14.9 (nl 7.0 31.4 ng/mL)
75 (nl 87–318 nmol/L)
19 (nl 20–60 mg/dL)
<7 (nl 8–30 nmol/L)
2.3 (nl 2.1–21.7ng/mL)
19.8 (nl 13.0–47.8 ng/mL)
7.3 (nl 5.7–19.9 mg/L)
<1.0 (nl > 4.3 mg/L)
0.77 (nl 0.35–4.94 UIU/mL)
2.6 (nl 3.5–5.0 mg/dL)
8.3 (nl 8.5–10.5 mg/dL)
2.5 (nl 2.7–4.5 mg/dL)

CSF Color
CSF Nucleated cells
CSF RBCs
CSFS Lymphocytes
CSF Glucose
CSF Protein
VDRL
RPR
Lyme
CMV
Herpes Simplex I+II

Colorless
1 (<5/uL)
4
15%
54 (40–70mg/dL)
37(15–45mg/dL)
Nonreactive
Nonreactive
Undetected
Undetected
Negative

NEUROCASE

3

Figure 1. MRI of the brain with DWI sequence showing restricted diffusion in the genu and splenium of the corpus callosum with a corresponding hypo-intense
region on ADC sequence. T1 sequence with hypo-intensity in the genu and splenium with corresponding hyper-intensity on T2 and FLAIR. A contrasted study did
not show enhancements (not shown).

the corpus callosum on diffusion weighted images (DWI)
and a corresponding hypo-intense region on apparent diffusion coefficient (ADC) sequences (Figure 1), as well as T1
sequence with hypo-intensity in the genu and splenium
with corresponding hyper-intensity on T2 and FLAIR
(Figures 2 and 3). MRI findings in MB have been reported
to include T1-weighted hypo-intensity and T2-weighted and
FLAIR hyper-intensity within the corpus callosum, specifically of the splenium. Acute cases of MB also show
restricted diffusion on DWI sequence (Logan et al., 2016).
MRI brain imaging revealed abnormalities compatible with
MB. In regard to other possible disorders that may reveal
similar images and a similar clinical presentation, she had
no risk factors for stroke; there was no trauma or other
disorders that could have produced diffuse axonal injury.
Her CSF evaluation revealed no oligoclonal bands nor

Figure 3. FLAIR sequence demonstrating a possible lesion within the frontal
lobe corresponding to Exner’s area.

Figure 2. T1 sagittal sequence demonstrating abnormal signal in genu and
splenium of the CC.

elevated IgG index, as well as no prior neurological symptoms, and she had no other MRI lesions consistent with a
diagnosis of multiple sclerosis. CSF was also without atypical
cells on cytometry or flow cytology, which would have
raised concern for central nervous system (CNS) lymphoma.

4

T. KESAYAN AND K. M. HEILMAN

When the diagnosis of MB disease was made she was
treated with a 5-day course of intravenous methylprednisolone 1 g/day and with 500 mg IV thiamin daily for 5 days,
followed by a 21 day course of daily IV multivitamin cocktail,
which contained 100 mg thiamin and 1 mg folic acid. After
several days of treatment, she improved, was more verbal, and
explained that she drank at least one bottle of red wine every
day for the past year or so.
After several weeks, examination revealed an alert woman,
who was oriented to herself, the date, her location, and the
circumstances of her hospitalization. She was able to follow
complex commands without difficulty, and spoke in sentences
fluently without paraphasic errors or other deficits; her repetition was also intact. She knew her left from her right, and
correctly identified the examiner’s left from his right. She
could name her fingers. Examination of her cranial nerves
revealed no deficits. On motor examination, she was thin,
and had a faint high frequency fine tremor in her hands and
fingers when her arms were extended in front of her at 90°.
Her tone was normal. She had full strength throughout.
Minimal endpoint ataxia was noted on finger-to-nose testing
in both hands, and with heel-to-shin testing in her feet. There
was a decrease to fine touch, temperature, vibration, and
pinprick in her feet and ankles, extending to several inches
above her ankles in both lower extremities. Her reflexes bilaterally were 3+ at the biceps, brachioradialis, patella, and at the
Achilles tendon. Her stance was slightly wide, and her walking
was cautious but without an obvious deficit.
Testing of praxis, graphesthesia, writing, and stereognosis
were conducted during the 26th day of the patient’s hospitalization after her cognitive status had significantly improved.
Her performance was videotaped by T.K and scored by T.K and
K.M.H. Permission for videotaping was obtained via Tampa
General Hospital Standard Medical Media Consent for
Education and Research. When testing her for graphesthesia,
her left hand was tested first. With this woman’s eyes closed,
the examiner wrote eight different numbers on each the
patient’s palms, and she was asked to identify each number
after it was written. She identified all numbers correctly. The
examiner also placed the following objects in the patient’s
hand, while her eyes were closed, and asked her to identify
them: pencil, bottle cap, paper clip, credit card, scissors, screw,

and a size AAA battery. Both hands were used in random
order. She identified each item correctly in both hands.
Writing was tested by asking the patient to write her name
and the numbers 4, 8, 65, 792 with her left and right hands.
She was also asked to write the sentence “Today is a beautiful
day” with her right hand and the sentence “I am going home
today” with her left hand. The patient’s handwriting sample is
shown in Figure 4. Prior to writing with her left hand, she
placed the paper at an angle such that the right top corner of
the paper was higher than the left. There was a large difference between her writing performance with her right and left
hands. Whereas, for the most part the words, numbers, and
letters written with the right hand can be recognized, only a
few letters and numbers written with the left are legible. It is
also apparent that with her left hand she repeatedly
attempted to correct her errors.
To learn if this patient, who appeared to have a splenial
lesion had hemialexia, the patient was also asked to read a set
of 16 compound words, for example “doghouse” and “keyboard,” which were presented to her at eye level, in her midline, and at about 2 feet away from her eyes. She read all
correctly. She was also asked to spell her name and several
words, which she performed correctly. She was also able to
recognize words spelled aloud by the examiner.
LKA was tested in both her right and left hands by having
her perform a coin rotation (Hanna-Pladdy, Mendoza,
Apostolos, & Heilman, 2002), using the method described by
Falchook (2015) and Hill et al., (2010) (Falchook et al., 2015; Hill
et al., 2010). She was first shown how to rotate a nickel between
her thumb, forefinger, and middle finger, and was asked to
rotate this coin as rapidly as possible for 10 s. Each hand was
tested five times. The score was the number of 180-degree
rotation of the nickel in 10 s. With her left hand, she rotated
the nickel to an average of 7.4 times (trials: 6,7,8,8,8 rotations),
and with her right hand to an average of 6.4 rotations (trials:
4,10,7,5,7). She dropped the nickel once during the fourth trial.
Standardized data using a U.S. quarter shows that during a 10-s
period the dominant hand performs an average of 13 rotations
and the nondominant hand too has an average of about 12
rotations (Hill et al., 2010). Therefore, this patient’s performance
on this task was somewhat impaired, suggesting that she has
an LKA of her right and left hands.

Figure 4. The patient’s handwriting sample. The patient’s name is blocked in the handwriting sample of both hands.
[To view this figure in color, please see the online version of this journal.]

NEUROCASE

IMA was tested by using the Apraxia Screen of TULIA (AST)
(Vanbellingen et al., 2011, 2010). In addition to the test items on
the AST, the patient was also asked to make believe to pantomime the movements made when she was scrambling eggs
and slicing a loaf of bread with a knife using her left and right
hand. She was also asked to imitate pantomimes performed by
the examiner, who performed the actions described in the
TULIA screen and the two additional actions mentioned above.
The patient did not have IMA; she was able to correctly
pantomime to command and imitate the use of a hammer, a
knife, a toothbrush, and a whisk along with correctly doing the
remainder of tasks in the AST. However, when pantomiming
how to use a pair of scissors, as if she was holding them in her
hand, to cut a piece of paper, she briefly held her index and
middle finger as if they were the blades of the scissors, and
made a cutting motion with her fingers. She made this error
with her left and her right hand until eventually changing the
position of her hand to resemble a correct position for holding
a pair of scissors. However, healthy participants often initially
make this body part as object error, until corrected (Raymer,
Maher, Foundas, Heilman, & Rothi, 1997).
To test for conceptual apraxia, the patient was shown pictures
of four uncompleted tasks (e.g., a screw is half way screwed into a
piece of wood), and was also shown several pictures of different
tools, one of which is the correct tool (screwdriver) and was
asked to pick the correct tool to complete the job. She was also
asked to pick the tool to complete tasks that were verbally
described to her. She performed these tasks without errors.
The patient was examined by T.K. again, approximately
1 year after she was initially evaluated by him. This follow-up
examination was again videotaped, and was afterward
reviewed by T.K and K.M.H. She was oriented to her herself,
the date, her location, and circumstance. She correctly followed three step commands, could normally repeat sentences,
and had fluent speech without paraphasic errors. Her recent
and remote memory was intact, and she could recall two of
three words after a 5-min delay. Her cranial nerve examination
was normal. She had no tremor of her hands or fingers at rest
or when extended outward at 90° from her torso. Her strength
was intact in her fingers and wrists, as well as the remainder of
her upper limbs. No ataxia or dysmetria was noted with fingerto-nose testing. Sensation was intact to fine touch pinprick,
vibration, and temperature in both of her upper limbs.
LKA was again tested with the coin rotation test, as
described above. With the right hand, she had an average of
8.2 rotations in 10 s (trials: 6,7,9,9,10), and with the left hand
an average of 8.4 rotations (7,9,8,10,8). In addition, repeated
testing again revealed that she did not have an IMA.
Her ability to write with the right and left hands was again
tested, but in a more comprehensive manner. Spontaneous
writing with her left hand was tested by presenting her with
the “cookie theft” picture from the Boston Diagnostic Aphasia
Examination and asking her to write a sentence about what she
sees (Roth, 2011). Spontaneous writing with her right hand was
assessed by showing her the “picnic scene” picture from the
Western Aphasia Battery and asking her to write a sentence
about what she sees (Kertesz, 1982). As she verbally explained,
with the left hand she intended to write “A family is doing
dishes and mom made a mess” and with the right hand she

5

wrote, “A Family is picnicking + Flying Kites with the Family
dog.” The writing with the left hand, for the most part, is totally
illegible, with impaired production of spatial features of the
letters. Her writing with her right hand was legible. Several
words were incorrectly capitalized, and she wrote using a combination of print and cursive letters. She used the plus sign, +,
instead of the word “and” when writing with both hands.
She was also asked to write to dictation with the right hand
the word “apple”, the phrase “black coffee,” and the sentence
“Close the door.” She was asked to write with her left hand the
word “shirt” the phrase “green light,” and the sentence “Turn
on the lights.” During this writing to dictation task, she again
revealed impaired grapheme production when writing with
her left hand. Although severely impaired, the left hand writing to dictation appears to be less impaired than her spontaneous writing (Figure 5).
Spatial agraphia is characterized by an impairment of visuospatial skills. For example, patients with spatial agraphia might
write only on one side of a paper. They might be impaired in
writing horizontally in respect to the top and bottom edges of
the paper and the might improperly space their letters or words
(Ullrich & Roeltgen, 2012). When our patient attempted to write
with her left hand (Figure 4) as she moved her hand across the
page from left to right, her writing progressively moved
upward, toward the top of the page. Thus, it appears that in
addition to the apraxia agraphia of her left hand, she also had a
form of spatial agraphia with her left hand.
She was asked to write with her left hand on paper that had
horizontal lines (Figure 5(e,f)) (Ullrich & Roeltgen, 2012), “Today
is a beautiful day.” and with her right hand she was asked to
write, “I’m going home today. She was also asked to write any
sentence she wishes with each hand on the lined paper. With
her left hand she attempted to write “Apple juice is in my cup.”
and with her right hand she wrote “I see star fish.” When writing
with her left hand she continued to make errors in the constructions of graphemes (apraxic agraphia). However, her
attempted writing was now horizontal, and there were no
obvious inappropriate insertions of blank spaces between graphemes. The writing with her right hand on these horizontal
lines remained horizontal. On the examination 1 year after, she
also positioned the paper at an angle prior to writing with her
left hand on several trials (Figure 5), and while writing, there did
not appear to be any sloping upward.
To evaluate her ability to copy written material, she was asked
to copy a word with each hand presented to her from 1 foot
away in 14 point type, as well as a sentence presented to her
from 6 feet away in 50 point type. With the left hand, she was
asked to copy the word “orange” and the sentence, “The dog
likes to play in the park.” With her right hand, she was asked to
copy the word “purple” and the sentence, “There are many fish in
the sea.” Although copying with her left hand is impaired, her
copying with her left hand is more legible than her spontaneous
writing with her left hand. In addition, when copying with her
right hand, she twice crossed out the letter “a” that she initially
wrote in cursive and replaced these cursive letters with a copy of
the letter “a” as it appeared on the typed paper.
She was able to spell the words “pen, foot, finger, computer” aloud without any errors. She was also able to type,
without errors, on a wireless computer keyboard “television”

6

T. KESAYAN AND K. M. HEILMAN

Figure 5. a1. The patient was shown the ‘cookie theft’ picture from the Boston Diagnostic Aphasia manual, andasked to rite a sentacne about what shee sees with her left
hand. a2: She was shown the ‘Picnic scene’picture from Western Aphasia Battery and asked to write a sentence about what she sees with her righthand. b1: The patient was
asked to write down the word or phrase the examiner said with her left hand,and dictated the following: “shirt; green light; turn on the lights”. b2: The patient was asked to
writedown the word or phrase the examiner said with her right hand, and was dictated the following: “apple;black coffee” close the door.” c1: the patient was instructed to
write on paper with horizontal lines; withher left hand she was asked to write the sentence “today is a beautiful day” and also any sentence shewould chose; she wrote
“Apple juice is in my cup.” c2: she was asked to write the sentence “I’m goinghome today” and another sentence of her choosing with the right hand on paper with
horizontal lines;she wrote “I see start fish.” d1: She was asked to copy the word “orange” which as presented one footaway from her eyes and was typed in 14 point font
with the left hand. Also with the left she was askedto copy the sentence “The dog likes to play in the park” which was presented to her from six feet awaytyped in 50point
font. d2, similar to D1 se was asked to copy with the right hand “purple” presented onefoot away typed in 14 point font, and the sentence “There are many fish in the sea”
presented to herfrom six feet away typed in 50 point font. e1: The patient was asked to close her eyes and write thesentence “It will rain today” with the left hand. e2: She
was asked to close her eyes and write thesentence “It is cold outside.”

and “nice to meet you” with her left hand and “camera” and “I
want to go home” with her right hand.
We examined several examples of our patient’s handwriting
with the right hand from the year prior to her hospitalization
(Figure 6). She did not have any examples of her handwriting
with her left hand from prior to her hospitalization. Her writing
with the right hand prior to her hospitalization appears to be
similar to the writing with the right hand tested 1 year after her
hospitalization.

Discussion
This right-handed woman with Type B MB disease who on
brain imaging revealed damage to the genu and the splenium

of her corpus callosum revealed an apraxic agraphia of her left
but not her right hand. She produced poorly formed graphemes, and demonstrated an inability to make accurately
sequenced motions to form these graphemes. She demonstrated apraxic agraphia with her left hand when writing
spontaneously, to dictation, when copying, when writing on
a horizontal line, as well as when writing with her eyes closed.
There does not appear to be a significant difference in her
writing ability with nouns compared to verbs. She was able to
type and spell aloud without any impairment; she had no
evidence for a linguistic agraphia.
She appeared to perform slightly better when copying text
with her left hand compared to writing to dictation, and even
better when compared to spontaneously writing with her left

NEUROCASE

Figure 6. Handwriting samples of the right hand from prior her presentation
with MB disease.

hand. People can copy written languages, such as Arabic or
Hebrew, without knowledge of the shape of the graphemes in
these languages or the knowledge of how to program the movements need to make these graphemes. Copying, in some respects
would be more like drawing than writing, and this improvement
in writing with copying has been shown in prior reports of
patients with apraxic agraphia (Valenstein & Heilman, 1979).
She had intact graphesthesia and stereognosis of both
hands and did not have an IMA of either hand. She was able
to correctly read compound words, spell, and type. Although
our patient appeared to have some evidence of an LKA initially, it was her right hand performance that was poorer than
her left hand, but she had apraxic agraphia only of her left
hand suggesting that her apraxic agraphia could not be attributed to an LKA. In addition, on the follow-up examination,
both of her hands performed equally on the coin rotation task,
and there was no tremor noted with this task. She did have
intermittent tremor with her left hand when writing, but not
during other portions of her examination. This tremor was not
present during all parts of her left hand writing examination,
and therefore, it does not appear to have contributed to her
impaired construction of written graphemes.
Margolin and Binder (1984) described a left-handed man
who had an extensive right hemisphere stroke and in addition
to an apraxic agraphia also revealed spatial agraphia. On our
patient’s initial evaluation, when attempting to write with her
left hand, this patient demonstrated aberrant spatial orientation of her writing on the paper, but she did not demonstrate
this spatial agraphia when writing with her right hand. As
mentioned, on the initial examination of her handwriting
with the left hand, prior to writing she placed the paper at
an angle, with the top of the paper placed rightward, in
respect to her body and her writing sloped upwards. On the
examination 1 year after, she also positioned the paper at an
angle prior to writing with her left hand on several trials
(Figure 5); however, while writing, there did not appear to
be any upward sloping. This dissociation suggests that it was
not the placement of the paper that induced her spatial
agraphia with upward sloping. When providing horizontal
lines on the paper, the patient did not show this upward

7

sloping of her writing, suggesting that this upward deviation
may have been related to inattention. When writing with her
left hand perhaps she did not attend to the edges of the
paper. Her failure to attend to the edges of the paper might
be related to her difficulty in writing with her left hand. As she
is aware of her impairment, perhaps she increases the focus of
her attention to the actions performed by her left hand and
this increase in focused attention led to a decrease in global
attention with unawareness of the paper’s edges. This hypothesis, however, cannot explain why she deviated upward and
further research is essential to learn if there are hand-hemispheric up-down action biases.
Several reports of agraphia of the left hand in the absence
of aphasia have been described. For example, Liepmann and
Maas (1907) described a patient who developed left upper
limb IMA as well as agraphia with the left hand, and on
postmortem examination was found to have a lesion in the
anterior four fifths of the corpus callosum. These authors
postulated that this lesion disconnected the left hemisphere
mediated movement formulas from the right hemisphere’s
motor control of the left arm, hand, and fingers (Liepmann &
Maas, 1907). However, Liepmann and Maas’s patient also had
a left frontal lesion and his right arm was hemiparetic and thus
could not be tested to learn if this was a callosal disconnection
apraxia. There have been several other similar reports of left
hand apraxia and agraphia with a callosal lesion (Dejerine &
Andre-Thomas, 1912; Geschwind & Kaplan, 1962).
Unfortunately, the agraphia in these cases was not fully
described, and thus it is unclear if the agraphia was apraxic
or linguistic. The patient with a callosal disconnection
described by Watson and Heilman (1983), however, did reveal
an IMA and apraxic agraphia of her left upper limb (Watson &
Heilman, 1983). Different from the case reported by Watson
and Heilman whose callosal lesion injured most of the anterior
two-thirds of her corpus callosum, the woman described in
this report had her lesions restricted to the genu and splenium
of the corpus callosum and had an apraxic agraphia in the
absence of an IMA.
Heilman and colleagues (1973) described a left-handed
man who had used his right hand for writing and who had a
lesion in the right hemisphere of his brain with a left hemiplegia. He had preserved language, but did reveal an IMA and
LKA of the left hand, as well as a left hand agraphia with
preserved spelling (Heilman et al., 1973). The authors posited
that although this left-handed man used his right arm and
hand for writing, his right hemisphere was dominant for motor
programming and the lesion in this hemisphere damaged or
disconnected these motor programs from the intact left hemisphere. The following year they described a right-handed man
who had a stroke of his left hemisphere. He had a right
hemiparesis and an IMA. In spite of having intact speech, he
had inability to write with his left hand (Heilman et al., 1974).
This patient had preserved ability to spell, and his agraphia
was somewhat improved when copying letters (1974).
Imaging confirmed a left MCA territory infarction. As in their
paper published the prior year, the authors again argued that
the lesion destroyed the movement representation important
in programming the production of written letters and words,
an apraxic agraphia. Later Valenstein and Heilman described

8

T. KESAYAN AND K. M. HEILMAN

another patient who was left handed and developed a lesion
in the right parietal lobe who had agraphia as well as apraxia,
but not aphasia. His spelling and his ability to correctly type
words when using a typewriter were intact (Valenstein &
Heilman, 1979).
Prior research on patients with IMA suggests that the
supramarginal gyrus contains the spatial–temporal representation for transitive and intransitive movements and lesions of
this area cause IMA (Heilman & Rothi, 2012). However, these
spatial–temporal representations have to be transcoded into
movement programs. Moreover, the convexity premotor cortex, as well as the supplementary area, appears to be important in converting the spatial representations of transitive and
intransitive movements, stored in the left inferior parietal lobe,
into motor programs. Therefore, lesions in the premotor cortex or the connecting fasciculi can also cause an IMA. As
discussed above, apraxic agraphia can occur in the absence
of IMA, and IMA can occur in the absence of apraxic agraphia.
This dissociation provides evidence that these two movement
programing networks are, at least in part, independent.
However, these two networks may have a similar organization.
Pure apraxic agraphia has been reported with injury to
the parietal lobe graphemic area (Ullrich & Roeltgen, 2012).
Support for the postulate that this area stores the spatial
grapheme representations used to program motor-writing
patterns of letters comes from observation that with
damage to this area writing with the hand and fingers is
impaired, but writing using a typewriter or anagram letters
is preserved. In addition, with injury to this area there is
defective letter imagery (Crary & Heilman, 1988). Like the
other purposeful movements mentioned above, the spatial–temporal representations of letter and words have to
be transcoded into movement programs. In 1881, Sigmund
Exner described an area in the left middle frontal gyrus
that he thought plays a critical role in writing. He called
this area the “graphic motor image center” (Exner, 1881).
Cortical electrical stimulation of this area produces impairment in handwriting without interfering with other hand
movements, and functional MRI has shown activation of
the left Brodmann’s Area (BA) 6 with handwriting (Roux
et al., 2009). Furthermore, fMRI has revealed that Exner’s
area, or the graphemic/motor frontal area, appears to be
the only one of several areas thought to play a role in
writing (Planton, Longcamp, Péran, Démonet, & Jucla,
2017). Thus, it appears that this graphemic/motor frontal
area is provided with the spatial–temporal information
about the structure of letters from the left parietal lobe,
and this frontal area converts these representations into
motor programs that sequentially activate the specific
areas of the motor cortex important for making the movements required for written letter production. Therefore,
with damage to this area patients have been reported to
have an inability to write but have preserved ability to
correctly spell words (Keller & Meister, 2014). Although
this patients had a greater impairment when writing with
her left than right hand, this patient did exhibit some
deficits when writing with her right hand. There are alterations in graphic strokes as well as changes in letter size
and a mix of print and cursive components in both the

patient’s original and follow-up hand writing samples.
These errors, however, were present in the sample of writing performed prior her hospitalization and therefore were
not likely the result of MB disease.
The midbody of the corpus callosum transmits the motor
programming information from the left hemisphere to the
right hemisphere that is important for making transitive and
intransitive movements of the left upper limb (Acosta et al.,
2014). However, when writing with left upper limb, the letter
movement programs stored in Exner’s area of the left hemisphere are probably transmitted through the genu of the
corpus callosum. Therefore, this woman’s injury to the genu
of the corpus callosum may have been responsible for the
agraphic apraxia of her left upper limb. However, additional
studies are essential to further test this hypothesis.

Disclosure statement
No potential conflict of interest was reported by the authors.

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