(Stroke. 1997;28:1755-1760.)
© 1997 American Heart Association, Inc.
Articles |
Motor Behavior in Stroke Patients With Isolated Medial Frontal Ischemic Infarction
From the Neurology Service of the Hospital Clínic University, Barcelona, Spain (A.C., J.V.-S., E.T.), and the Department of Neurology of the Neurological Institute, Columbia–Presbyterian Medical Center, New York, NY (R.S.M., J.P.M.).
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Abstract |
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Background and Purpose Current interpretation of hemiparesis in anterior cerebral artery infarction holds that whereas leg weakness correlates with destruction of the corticospinal tract at the paracentral lobe, faciobrachial symptoms indicate extension of the infarct to the upper lateral convexity or to subcortical structures, where the corticospinal tract subserving the arm would be interrupted. We analyzed the motor behavior in eight patients with purely medial hemispheric infarctions who had face, arm, and leg involvement.
Methods In addition to careful clinical testing, we performed neuroimaging or pathological studies to exclude the involvement of the primary motor cortex or subcortical structures. Motor function was further tested in three patients by studying the reaction time to an auditory stimulus and by stimulating the motor cortex and the cervical and lumbar spine with a magnetic stimulator.
Results All patients had signs of motor neglect, such as lack of spontaneous movement in the upper limb, unilateral reaction to pain stimuli, clumsy voluntary movements, or motor impairment on bimanual tasks. Electrophysiologically, we found absent or poor voluntary activity in both upper and lower limbs contralateral to the infarction. However, whereas cortical stimulation showed absent responses in the lower limb, it disclosed normal latencies in the upper limb, indicating that the corticospinal tract to paretic muscles of the upper limb was intact.
Conclusions Our findings suggest that faciobrachial symptoms in purely medial hemispheric infarctions in the anterior cerebral artery territory reflect motor neglect caused not by involvement of primary motor pathways but by damage to medial premotor areas.
Key Words: cerebral arteries • cerebral infarction • hemiplegia • magnetics • motor activity
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Introduction |
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Infarction in the territory of the ACA generally results in weakness restricted to the contralateral leg, reflecting damage to the corticospinal tract at the paracentral lobule or its corticofugal fibers.1 2 In some instances the distal arm and face may also be involved, either in isolation3 or with concomitant leg weakness.4 5 In those cases, the mechanisms responsible for faciobrachial symptoms are not well elucidated. A recent review of this subject6 reported that when the motor deficit is not restricted to the lower limb, faciobrachial symptoms could be explained by extension of the infarction to the lateral convexity, where fibers originating from the primary motor cortex would be damaged. Another explanation for this motor profile holds that upper limb weakness could ensue from the concomitant infarction of the genu and/or anterior third of the posterior limb of the internal capsule, as a result of occlusion of small penetrating arteries that arise from the proximal segment of the ACA or the distal internal carotid artery.2 7 To our knowledge, however, there is no convincing evidence of such a mechanism in humans. Recent clinical series of patients with pure motor hemiplegia have shown that infarctions restricted to the genu or posterior limb of the internal capsule most frequently resulted in hemiplegia (face, arm, and leg).8 The same authors also observed a wide variation of motor syndromes in patients with isolated capsular infarctions, lessening support for the classic view of a homunculus in the internal capsule with face, arm, and leg displayed in a strict anteroposterior distribution.8 Based on our current understanding of the cortical origin of the primary motor cortex, its subcortical course, and its localization in the internal capsule,9 10 it is our contention that neither capsular infarction nor involvement of the lateral convexity explains satisfactorily faciobrachial involvement in ACA infarctions restricted to the medial surface of the frontal lobe. The aim of our study was to test the hypothesis that upper limb dysfunction is not the consequence of an interruption of the corticospinal fibers subserving the upper limb but reflects defective supramotor planning, unilateral hypohinesia, or motor neglect due to damage of medial premotor areas.
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Subjects and Methods |
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Subjects in this series included eight right-handed patients with first-ever ischemic stroke restricted to the medial frontal lobe supplied by the ACA who had face and arm equally or more severely affected than the leg at the time they were examined by one of the authors. Patients whose ACA infarction or any other associated lesion affected the contralateral medial frontal lobe or the ipsilateral internal capsule, caudate, basal ganglia, pons, or lateral convexity were not included in the study to avoid the confounding effects of lesions located outside the anatomic region of interest. All patients had a brain CT scan performed the day of hospital admission. At least 1 week after stroke onset, a 1.5-T brain MRI was performed in six patients to better delineate the boundaries of the infarction and to exclude the presence of small lesions that could have passed unnoticed with CT imaging. Scans were performed in the sagittal and coronal planes with T1 weighting and in the axial plane with proton density and T2 weighting, generating images that were 5 mm thick with an interslice gap of 2.5 mm (Fig 1
). A second brain CT scan was obtained 1
week after stroke onset in the remaining two patients because
claustrophobia and a cardiac pacemaker, respectively, prevented the
acquisition of a brain MRI. In one patient, gross and microscopic
pathology was also available from autopsy. The topography of the
infarctions, as detected on MRI or CT scan, was analyzed by a
neuroradiologist blinded to the clinical data using the brain atlas of
the Damasios.11
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To circumvent current controversies concerning the precise boundaries of functional cortical fields in the frontal lobe, we referred to these functional cortical fields as medial premotor areas, as recently recommended.12
Electrophysiological Evaluation
The electrophysiological part of the
study was approved by the local internal review board, and informed
consent was obtained from the patient's relatives.
Electrophysiological studies were performed in
three patients (patients 1, 2, and 3). Patient 4 could not be studied
because he died prematurely. The four patients admitted to one of the
institutions were not evaluated
electrophysiologically because the
technique was not available. We measured simple reaction time as the
onset latency of the EMG activity recorded in the abductor pollicis
brevis, biceps brachii, and tibialis anterior muscles by surface
electrodes. Subjects were instructed to activate their hand or
foot muscles as soon as possible after hearing an auditory stimulus
delivered by discharging the magnetic coil of a magnetic stimulator
held 10 cm above the subject's head. In one patient, in addition to
recording the EMG activity, we also recorded displacement
of the moving limb by an accelerometer attached to the thumb or to the
dorsum of the foot.
We measured the functional integrity of the corticospinal tract to distal muscles of the upper and lower limbs by stimulating the motor cortex and the spinal cord with a cortical magnetic stimulator (Novametrix 200). For thenar muscles, focal cortical stimulation was accomplished by applying a "figure 8" coil on the scalp positions overlying the cortical motor strip.13 For tibialis anterior muscles, we used a round coil centered over the vertex. Spinal cord stimulation was accomplished by applying the coil over the cervical spine, centered on C7, for the upper limbs, and over the lumbar spine, centered on L1, for the lower limbs. CMCT was calculated by subtracting the latency of the thenar or tibialis anterior responses obtained by spinal cord stimulation from those obtained in the same muscles by cortical stimulation.
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Results |
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Clinical Findings
The main features of the motor phenomena manifested by the patients are presented in Table 1
. With the exception of 3 patients who
showed moderate hemiparesis, the remainder of the patients disclosed at
stroke onset a total lack of voluntary movement in the contralateral
limbs that prevented adequate testing of motor praxis and
performance of bimanual tasks. Movement could not be coaxed by
the examiner despite strong verbal and gestural commands. Pain reaction
was also defective or absent with the limbs contralateral to the
lesion. In patients who had less than total hemiplegia at stroke onset
and in 2 additional patients during the recovery phase (patients 1 and
3), we observed that they were able to generate slow, hypometric, and
clumsy upper limb movements after strong prodding, despite a continuing
lack of spontaneous movement. As shown in Table 1, tendon reflexes and
muscular tone had no predictable pattern among studied patients. Most
patients demonstrated that motor performance worsened compared
with their baseline capacities if bimanual tasks were requested. A
grasp reflex was observed in half of the patients, and compulsive
manipulation of tools consistent with a frontal alien hand
syndrome was detected in patient 8.14 15 Motor recovery
was variable among patients, although this could be partially due
to the uneven length of clinical follow-up. While most patients
demonstrated some degree of motor recovery of the faciobrachial
deficits during the first weeks, complete recovery was seen only in 1
patient; 3 additional patients showed a total absence of motor recovery
at 2, 3, and 4 weeks, respectively. Patients 1 and 4 developed at
stroke onset and 4 weeks after stroke, respectively, a focal motor
seizure consistent with the activation of the contralateral
SMA.
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Other associated neurological findings encountered in these patients included those expected after ACA infarctions, such as gaze preference in 4 patients, mutism or reduced spontaneous speech in 4, aphasia in 3, visual hemineglect in 3, hypoesthesia in 2, urinary incontinence in 1, and left ideomotor apraxia in 1.
Pathological Findings
Patient 4 died 40 days after stroke onset. On neuropathological
examination the fixed brain weighed 1200 g. The circle of Willis
showed moderate atherosclerotic disease; with the exception of the
distal right ACA, the rest of the arteries were patent, including the
anterior communicating artery and Heubner's artery. On serial sections
of the ACA a large plaque was seen in the A3 portion, with a thrombus
occluding the remainder of the lumen of the artery. One-centimeter
brain sections demonstrated an area of pale softening involving the
right posterior medial superior frontal gyrus with minimal involvement
of the deep hemispheric white matter. The lesion extended along the
genu of the corpus callosum, the gyrus cyngulate, the most anterior
part of the paracentral lobule, and the entire extent of the region
corresponding to the SMA. The head of the caudate, the pallidum, the
putamen, and the pons were normal, as well as the contralateral frontal
cortex.
Electrophysiological Findings
Data on reaction time and on responses recorded in thenar
and tibialis anterior muscles are summarized in Table 2. Examples of the EMG activity obtained
in reaction time experiments are shown in Fig 2. In patient 1 there was absence of any
EMG activity in the right biceps brachii and tibialis anterior muscles
(Fig 2A). In the right thenar muscles, a small burst of activity was
observed in a few trials at latencies of 700 to 800 milliseconds.
Reaction time was delayed in muscles of the left side compared with
normal individuals. In contrast to the poor voluntary activity of both
upper limbs, latencies of the motor evoked potentials to cortical and
cervical spine stimulation, as well as the CMCT, were normal in thenar
and biceps muscles of both sides (Fig 3).
The response in the right tibialis anterior was absent to cortical
stimulation but present at a normal latency of 18 milliseconds with
lumbar spine stimulation. The CMCT was normal in the left tibialis
anterior, as indicated in Table 2.
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Patient 2 was studied in a similar manner 1 month after stroke onset.
The reaction time experiment revealed absence of any EMG activity in
the right thenar muscles, biceps brachii, and tibialis anterior
muscles. As in patient 1, reaction time was delayed in muscles of the
left side compared with normal values. Furthermore, the EMG activity
recorded in the left thenar and biceps brachii muscles was not that
of the typical interference pattern but a sequence of small bursts (Fig 2B
). On cortical magnetic stimulation, motor evoked potentials were
obtained in the thenar muscles bilaterally at normal latencies. In the
right tibialis anterior, the response to cortical stimulation was
absent, whereas the response to lumbar spine stimulation occurred with
a normal latency of 17.3 milliseconds. The CMCT was normal in the left
tibialis anterior.
Patient 3 was also studied 1 month after stroke onset. In the reaction
time experiment, EMG activity was absent only in the left tibialis
anterior. The onset latency of the EMG activity was delayed in the left
thenar muscles and biceps brachii compared with the same muscles of the
right side, which had normal activation latencies. In the left biceps
brachii, despite the presence of EMG activity, no displacement was
registered by accelerometer recording (Fig 2C). Motor evoked
potentials to cortical stimulation were obtained in the biceps brachii
and thenar muscles of both sides with normal latencies. In the left
tibialis anterior, the response to cortical magnetic stimulation was
absent, whereas the response to lumbar spine stimulation occurred at a
latency of 17.5 milliseconds. Cortical stimulation produced normal
responses in the right tibialis anterior.
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The present study suggests that faciobrachial symptoms in purely medial hemispheric infarctions in the ACA territory reflect motor neglect caused not by involvement of primary motor pathways but by damage to medial premotor areas. Although small subcortical lesions may have been missed in the two patients with CT imaging data alone, no subcortical involvement was apparent in any of the other patients when MRI or pathology was available. Therefore, we are confident that the symptoms analyzed in the present study truly reflect acute ischemic damage restricted to the medial frontal lobe in humans.
Patients with medial frontal tumors may manifest symptoms that occasionally are difficult to differentiate from hemiparesis.16 Thus, it is not surprising that the syndrome has been described as hemiplegia,1 psychic hemiplegia,17 akinesia,18 or akinetic mutism.19
We observed that most patients were able to display at follow-up some motor function with the affected limbs if strongly prodded. However, whenever adequate testing was possible, lack of spontaneous movement, defective pain reaction, and abnormal motor performance on bimanual tasks persisted. This behavior has been previously referred to as unilateral motor neglect, bradykinesia evolving from a complete akinesia, relative anosodiaphoria, or motor extinction.18 20 21 22 23 24
There is general agreement that the long-term effects that follow medial frontal lobe lesions are subtle.18 25 However, this information is mainly derived from observations made in young epileptic patients after ablative procedures or in patients with brain tumors. On the contrary, the long-term effects of ACA infarction are mostly unknown. Most of our patients disclosed partial recovery of the upper limb abnormalities during the initial weeks after stroke. However, two patients disclosed faciobrachial deficits for longer periods of time. Interestingly, these two patients experienced partial seizures during the early phase of stroke, presumably originating in or involving the SMA, leading to the speculation that seizure activity was responsible for a more severe tissular damage. In agreement with our findings, permanent worsening of clinical symptoms has been also reported in stroke patients with early seizures and without the noticeable intervention of further ischemic lesions.26
All the patients included in this study had lesions restricted to the medial frontal cortex, where several medial premotor areas have been identified.25 However, to assign individual stroke symptoms to single functional medial frontal fields is hampered by the common arterial supply to these areas. Our current understanding of the functional role of medial frontal fields comes from human and animal studies involving electrical stimulation, cerebral blood flow measurement, or ablative procedures.27 Human studies have shown cerebral blood flow increases in the SMA region during planning of segmental movements, suggesting that a higher-order, supramotor center is involved in the generation and programming of complex movements.28 Positron emission tomographic studies have also suggested that the SMA region plays an important role in the execution of complex sequential finger movements,29 the initiation of movements triggered by sensory cues,30 and the initiation of movement, irrespective of task complexity.31 32 The anterior part of the SMA region is concerned with more complex (ie, planning and decision) components of movement, whereas the posterior part of the SMA region is more closely linked with corticospinal pathways involved in self-paced or internally generated movements.30 Despite the influential role of the medial frontal lobe for normal motor functioning, it remains widely accepted that a lesion to the corticospinal tract is needed to explain the hemiparesis that can be observed in patients with ACA infarctions.33 The fact that some of our patients had increased tone and hyperactive tendon reflexes would also argue in favor of upper motor neuron involvement. However, our patients better complied with the motor behavior described in subjects with motor neglect, namely, lack of spontaneous movement, inadequate reaction to painful stimuli, and clumsy voluntary movements.20 It must also be noted that occasionally patients with motor neglect may also have clinical findings suggestive of pyramidal tract dysfunction, such as hyperactive tendon reflexes or a Babinski sign.20 Moreover, we provide radiological and pathological evidence that the lesions were medial to the functional area of the primary motor cortex where the upper limb is represented, and the cortical magnetic stimulation studies performed in three of them further disputed the role of the corticospinal tract in the genesis of the upper limb motor symptoms.
Transcranial cortical magnetic stimulation of the motor cortex has been established as a useful tool for examination of the central nervous system.34 35 It generates descending volleys in the corticospinal tract by producing transynaptic excitation of the pyramidal cells after depolarizing cortico-cortical association axons. Therefore, if normal responses are detected in patients with cortical lesions, it is improbable that they are generated by deep stimulation of the corticospinal axons. In our patients the absent responses to cortical stimulation found in the lower limbs of the affected side indicated a functional interruption of the corticospinal tract.36 However, preserved normal cortical responses in the "paretic" upper limbs suggested that the traffic of nerve impulses in the corticospinal tract to thenar muscles was normal despite the prominent motor deficit. The delay or absence in execution of spontaneous or signal-triggered movements we observed may therefore be attributable to a functional impairment in neural structures lying upstream of the primary motor cortex, perhaps in areas related to premotor planning or initiation of motor acts. We also observed a delay in reaction time in the ipsilateral limbs of two patients with left-sided lesions. Our ipsilateral findings would further support the notion of dysfunction of motor association areas rather than primary motor tracts.37 These observations are also in agreement with recent functional MRI studies which showed that whereas the right primary motor cortex was activated by contralateral finger movements, the left motor cortex was activated by both ipsilateral and contralateral movements.38 However, we cannot exclude the possibility that our observations of laterality differences were due to an artifact of small sample size.
In summary, we provide anatomic, clinical, and electrophysiological evidence that the faciobrachial motor symptoms encountered in our patients with ACA infarctions do not indicate corticospinal tract weakness but unilateral motor neglect produced by injury to medial premotor areas or its connections. Whether variance in duration and intensity of this syndrome is related to anatomic differences, seizure activity after stroke, ischemic severity, or hemispheric asymmetry awaits confirmation from detailed longitudinal series. Since a better understanding of symptoms and signs can result in superior therapeutic strategies, including rehabilitation, we encourage the report of detailed clinicoanatomic studies aimed at clarifying the clinical findings derived from the lesion of the SMA region in stroke patients.
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Selected Abbreviations and Acronyms |
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Footnotes |
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Reprint requests to Dr A. Chamorro, Neurology Service, Hospital Clinic University, Villarroel 170, 08036 Barcelona, Spain.
Received March 13, 1997; revision received May 12, 1997; accepted May 13, 1997.
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