195

NeuroRehabilitation 33 (2013) 195–200
DOI:10.3233/NRE-130945
IOS Press

Motor recovery by improvement of
limb-kinetic apraxia in a chronic stroke
patient
Sung Ho Jang
Department of Physical Medicine and Rehabilitation, College of Medicine, Yeungnam University 317-1,
Daemyungdong, Namku, Taegu, 705-717, Republic of Korea. Tel./Fax: +82 53 620 3269;
E-mail: strokerehab@hanmail.net.

Abstract.
OBJECTIVES: We report on a chronic stroke patient who showed motor recovery by improvement of limb-kinetic apraxia (LKA)
after undergoing intensive rehabilitation for a period of one month, which was demonstrated by diffusion tensor tractography
(DTT) and transcranial magnetic stimulation (TMS).
METHODS: A 50-year-old male patient presented with severe paralysis of the left extremities at the onset of thalamic hemorrhage.
At thirty months after onset, the patient exhibited moderate weakness of his left upper and lower extremities. In addition, he
exhibited a slow, clumsy, and mutilated movement pattern during grasp-release movements of his left hand. During a one-month
period of intensive rehabilitation, which was started at thrity months after onset, the patient showed 22% motor recovery of the
left extremities. The slow, clumsy, and mutilated movement pattern of the left hand almost disappeared.
RESULTS: DTTs of the corticospinal tract (CST) in both hemispheres originated from the cerebral cortex, including the primary
motor cortex, and passed along the known CST pathway. The DTT of the right CST was located anterior to the old hemorrhagic
lesion. TMS study performed at thirty and thirty-one months after onset showed normal and similar findings for motor evoked
potential in terms of latency and amplitude of the left hand muscle.
CONCLUSIONS: We think that the motor weakness of the left extremities in this patient was mainly ascribed to LKA and that
most of the motor recovery during a one-month period of rehabilitation was attributed to improvement of LKA.
Keywords: Motor recovery, stroke, diffusion tensor tractography, transcranial magnetic stimulation, apraxia, limb-kinetic apraxia

1. Introduction
Stroke is a leading cause of major disability in
adults. Motor weakness is one of the most serious
disabling sequelae of stroke, with more than 50% of
stroke patients experiencing a residual motor deficit
[6]. Injury of neural tracts affecting motor function
is accompanied by motor weakness, however, apraxia
can also accompany motor weakness like symptoms.

Apraxia is defined as the inability to perform learned
skilled movements in spite of preservation of power,
sensation, and comprehension for execution of movements [9–11]. Limb-kinetic apraxia (LKA), one of
the apraxias, is defined as the execution disorder
of movements, resulting from injury of the premotor cortex (PMC) or the corticofugal tract from the
PMC with preservation of the corticospinal tract (CST)
[12, 19, 21, 26].

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S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

Diagnosis of LKA can be difficult because it is made
by clinical observation of movements with confirmation
of the CST state. Diffusion tensor tractography (DTT),
derived from diffusion tensor imaging (DTI), provides
a unique advantage for three-dimensional visualization
and estimation of the CST [13, 16, 17, 24]. Transcranial
magnetic stimulation (TMS) stimulates the neurons of
the CST and provides a unique advantage for estimating
the amount of CST fibers by measuring amplitude of
motor evoked potential (MEP) [27]. Therefore, TMS
could be useful for demonstrating change in the amount
of CST fibers.
In the current study, we report on a chronic stroke
patient who showed motor recovery by improvement
of LKA after undergoing intensive rehabilitation for a
period of one month, which was demonstrated by DTT
and TMS.

2. Case report
The standardized Motricity Index (MI) and Medical
Research Council (MRC) were used for determination
of motor function [2, 4]. The MI, with a maximum score
of 100, is a measure of the integrity of extremity motor
function. Reliability and validity of the MI are wellestablished [4]. The MRC score was used for evaluation
of motor function: 0, no contraction; 1, palpable contraction but no visible movement; 2, movement without
gravity; 3, movement against gravity; 4, movement
against a resistance lower than the resistance overcome
by the healthy side; and 5, movement against a resistance equal to the maximum resistance overcome by the
healthy side [2].
A 50-year-old, right-handed male patient presented
with severe paralysis of the left upper and lower extremities at the onset of thalamic hemorrhage (MI: 0). The
patient received conservative management at the neurosurgery department of a university hospital and then
underwent rehabilitation at a local rehabilitation hospital. However, he could not perform most daily activities
using his left hand and could not walk independently
without a cane. At thirty months after stroke onset, the
patient was admitted to the rehabilitation department
of a university hospital in order to undergo intensive
rehabilitation. At the time of admission, the patient’s
scores on the Mini-Mental State Exam and the ideomotor apraxia test were 28 (cut-off score <25) and 40
(cut-off score <32), respectively [3, 7]. According to
the Nottingham Sensory Assessment (The subscales for
tactile sensation (16, full mark: 20) and kinesthetic sen-

Table 1
Changes of motor function and the results of transcranial magnetic
stimulation in the patient
Duration from onset
MRC

MI

TMS

Shoulder abductor
Elbow flexor
Finger flexor
Finger extensor
Hip flexor
Knee extensor
Ankle dorsiflexor
Upper extremity
Lower extremity
Total
Latency (msec)
Amplitude (␮V)

Onset

30 months

31 months

0
0
0
0
0
0
0
0
0
0

3+
4
3+
3
3+
4
2+
65
57
61
22.3
4000

4+
5
4+
4
4+
5
4
84
83
83
22.7
4000

MRC: Medical Research Council, MI: Motricity Index, TMS: Transcranial magnetic stimulation.

sation (20: full mark: 24), he showed mild impairment
of somatosensory function [23]. The patient exhibited
moderate weakness of his left upper and lower extremities (MI: 61) (Table 1). In addition, he exhibited slow,
clumsy, and mutilated movements when performing
grasp-release movements of his left hand. He walked
with a pattern of spastic circumduction and severe
associated reaction of the left elbow. T2-weighted MR
images taken at thirty months after onset showed an
old hemorrrhagic lesion in the right thalamus, posterior limb of the internal capsule, and midbrain (Fig. 1).
The patient provided signed, informed consent and our
institutional review board approved the study protocol.
The patient participated in a comprehensive rehabilitative management program, including movement
therapy, dopaminergic drugs for improvement of
apraxia (ropinorole, 3 mg; bromocriptine, 10 mg; levodopa, 375 mg), antispastic drugs (baclofen 45 mg),
and neuromuscular electrical stimulation therapy of the
left elbow extensors, finger extensors, knee extensors,
and ankle dorsiflexors (two times, 20 minutes/time,
seven days/week). Movement therapy was performed
primarily for improvement of motor function, movement pattern of the left extremities, and postural control,
and was performed six days (Monday through Friday:
2.5 hours/day, Saturday: one hour/day) per week. During a one-month period of intensive rehabilitation, the
patient showed motor recovery of the left upper and
lower extremities of as much as 22% on MI (61–>83).
In addition, his slow, clumsy, and mutilated movement
pattern when performing grasp-release movements of
his left hand almost disappeared. He was able to walk
independently, showing marked improvement of spastic circumduction gait pattern and severe associated
reaction of the left elbow.

S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

197

A

R

B

R
R

C

A
10ms

30-month

1mV

10ms

31-month

1mV

Fig. 1. A. T2-weighted brain MR images show an old hemorrhagic lesion in the right thalamus, posterior limb of the internal capsule, and
midbrain. B. Diffusion tensor tractography for the corticospinal tract of the affected hemisphere at thirty months after onset was similar to that of
the hemisphere of the unaffected side. The old hemorrhagic lesion (arrow) was located posterior to the right corticospinal tract. C. Motor-evoked
potentials obtained from the left abductor pollicis brevis muscle at thirty and thirty-one months after onset showed similar latency and amplitude.

2.1. Diffusion tensor tractography
A 6-channel head coil on a 1.5 T Philips Gyroscan
Intera (Philips, Ltd., Best, the Netherlands) with
single-shot echo-planar imaging was used for acquisition of DTI data. For each of the 32 non-collinear
diffusion sensitizing gradients, we acquired 70

contiguous slices parallel to the anterior commissureposterior commissure line. Scanning was performed
from the cortex to the middle of the second cervical vertebral body. Imaging parameters were
as follows: acquisition matrix = 96 × 96; reconstructed to matrix = 192 × 192 matrix; field of view
= 240 mm × 240 mm; TR = 10,398 ms; TE = 72 ms;

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S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

parallel imaging reduction factor (SENSE factor) = 2;
EPI factor = 59; b = 1000 s/mm2 ; NEX = 1; and a slice
thickness of 2.5 mm (acquired isotropic voxel size
2.5 mm × 2.5 mm × 2.5 mm). The fiber assignment
continuous tracking (FACT) algorithm implemented
within the DTI task card software (Philips Extended
MR WorkSpace 2.6.3) was used in performance of
fiber tracking [24]. For CST analysis, a seed region of
interest (ROI) was placed on the CST at the anterior
pontomedullary junction on an axial slice and a target
ROI was drawn in the CST area of the anterior medulla
[14]. The termination criteria applied were fractional
anisotropy (FA) <0.2 and an angle change of >45
degrees [17].
Results of DTT of the right and left CST showed that
fiber tracts originated from the cerebral cortex, including the primary motor cortex, and passed along the
known CST pathway (Fig. 1-B). DTT of the right CST
was located anterior to the old hemorrhagic lesion.
2.2. Transcranial Magnetic Stimulation
A Magstim Novametrix 200 magnetic stimulator
with a 9-cm mean diameter circular coil (Novametrix
Inc.) was used in performance of TMS. Cortical stimulation was performed with the coil held tangentially
over the vertex. Stimulation of the left hemisphere
was provided by a counterclockwise current, and
stimulation of the right hemisphere was provided by
a clockwise current. Four motor-evoked potentials
(MEPs) were obtained from both abductor pollicis
brevis (APB) muscles in a relaxed state. Stimulation
intensity was set at the maximum stimulator output.
Each site was stimulated three times with inter-stimulus
intervals of >10 seconds, and MEP having the shortest
latency and the average peak-to-peak amplitudes was
adopted.
TMS study performed at thirty and thirty-one months
after onset showed similar MEP findings at the left
APB muscle (thirty months: latency- 22.3 msec; amplitude: 4000 uV), thirty-one months: latency- 22.7 msec;
amplitude: 4000 uV).

3. Discussion
Diagnosis of LKA is difficult because there are
no specific diagnostic tools; instead, it is dependent
on clinical observation of movements. The nature of
LKA has not been clearly elucidated, therefore, it has
been controversial. Summarizing previous studies, the

characteristics of LKA are as follows [5, 9, 12, 21,
22]: 1) awkward, clumsy, coarse, mutilated pattern of
execution of simple movements, confined mainly to
movements of the affected hand, 2) resulting mainly
from frontal lobe damage centered on the PMC or the
corticofugal tract from the PMC with preservation of the
CST, 3) no voluntary-automatic dissociation, 4) differentiation from concurrent limb weakness resulting from
injury of the CST is difficult because it is similar to the
motor weakness observed following CST injury, and 5)
normal conceptual knowledge of motor performance.
In this patient, we observed 22% motor recovery for
a period of one month from thirty months after onset.
We think that the motor weakness of the left extremities in this patient was mainly ascribed to LKA and
that most of the motor recovery during a one-month
period of rehabilitation was attributed to improvement
of LKA, for the following reasons. First, we confirmed that the CST in the affected (right) hemisphere
showed normal findings in terms of MEP parameters
(latency and amplitude) on TMS and configuration
on DTT [15]. However, the patient exhibited moderate motor weakness in the left extremities until thirty
months after onset. The clinical characteristics of left
hand movements (slow, clumsy, and mutilated) were
also compatible with those of LKA. However, because
the patient showed normal cognition for motor performance and a normal result on the ideomotor apraxia
test (20: cut-off score <32), we were able to rule out
ideational and ideomotor apraxia. Second, the patient
had a lesion around the CST in the posterior limb of
the internal capsule, which is known to related to the
corticofugal tract from the PMC, which is responsible for LKA [5, 8, 9, 12, 21, 25]. Third, he showed
rapid motor recovery for one month from thirty months
after onset, which is well-known as the plateau stage
of motor recovery in stroke patients. Considering the
amplitudes of MEP, which indicate that the fiber numbers of the CST in the affected hemisphere were not
changed between thirty and thirty-one months, we can
assume that the motor recovery was mainly attributed
to improvement of LKA. In particular, dopaminergic
drugs, which have been reported to be effective for
treatment of apraxia, appeared to have been effective
for improvement of LKA [18, 20, 28, 29].
To the best of our knowledge, only a few studies
using DTI have reported on LKA [1, 12]. In 2008, in an
investigation of changes in white matter in 21 patients
with corticobasal degeneration syndrome, Borroni et al.
reported correlation of limb apraxia with parietal atrophy and with FA reductions in parietofrontal associative

S.H. Jang / Motor recovery by improvement of limb-kinetic apraxia

fibers [1]. In addition, the limb-kinetic component of
apraxia showed correlation with reduction of hand
sensorimotor connecting fibers. Recently, Hong et al.
[2012] reported on a patient with ideomotor apraxia and
LKA following a cerebral infarct in the left frontal cortex [12]. They demonstrated the partial injuries of the
neural tracts from the PMC and superior longitudinal
fasciculus in the affected hemisphere that were responsible for LKA and ideomotor apraxia, respectively.
In conclusion, we report on a patient who showed
motor recovery during a one-month period between
thirty and thirty-one months after stroke onset. Using
DTT and TMS, we demonstrated that motor recovery was mainly ascribed to improvement of LKA.
Because LKA can accompany motor weakness like
symptoms, and it can be resolved by intensive rehabilitation, including dopaminergic drugs, diagnosis of
LKA is important in stroke rehabilitation. Therefore,
we believe that our results have important implications
for stroke rehabilitation. However, because it is a case
report, this study is limited. Conduct of further complementary studies involving larger numbers of cases
is warranted.

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Acknowledgments
This research was supported by Basic Science Research Program through the National
Research Foundation of Korea (NRF) funded by
the Ministry of Education, Science and Technology
(2012R1A1A4A01001873).

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