대 한 방 사 선 의 학 회 지 1991; 27(3) : 323~328 Journal of Korean Radiological Society. May. 1991

MR Imaging of N euronal Migration Anomaly

Hyun Sook Hong, M.D. , Eun Wan Choi, M.D. , Dae Ho Kim, M.D. , Moo Chan Chung, M.D. , Kuy Hyang Kwon, M.D. , Ki Jung Kim, M.D.

Department o[ RadíoJogy. Col1ege o[ Medícine. Soonchunhyang University

Introduction

Abnormalities of neuronal migration Sl re

characterized by anectopic location of neurons in the

cerebral cortex (1-9). This broad group of anomalies

includes agyria. pachygyria . schizencephaly.

unilateral megalencephaly. and gray matter

hcterotopia. Patients with this anomaly present

clinically with a variety of symptoms which are pro­

portional to the extent of the brain involved. These

abnormalities have been characterized pathologically

in vivo by sonography and CT scan (2. 3. 10-14.

15-21).

MR appears to be an imaging technique of choice

in evaluating these anomalies because it is capable

of exceptionally good differentiation between gray

and white matter. high contrast resolution .

m비tiplan와 display of the anatomy. and lack of

overlying bone artifact (1. 22-24).

The purpose of this paper is to describe the MR fin­

dings of neuronal migration anomaly.

Subjects and Methods

Eleven patients with neuronal migration

anomalies were examined with MR (10 patients) and

CT (one patient) from May 1989 to September 1990

because of seizure. mental retardation. developmen­

tal delay. enlarged head. and motor weakness. The

Index Words: Brain. abnormalities. 13. 14.

Brain ‘ MR imagings . 13 ‘ 1214

patients ranged in age from 5 months to 42 years with

a mean of 16 years. The mean age was skewed by

2 patients with schizencephaly who were 35 and 42

years old.

MR was performed with a 0:2T permanent type

(Hidachi PRP 20) . Slice thickness was 5mm with a

2.5mm interslice gap or 7.5mm thickness. Spin echo

axial images were obtained. including Tl weighted

images (TIWI) with a repetition time (TR) of

400-500ms and echo time (TE) of 25-40ms. in­

termediate images of TR/TE 2000/38 . and T2

weighted images (T2W l) with a TR/TE of 2000/110.

Occasionally. sagittal and coronal images were ob­

tained. Gd-DTPA enhanced Tl WI were 려so obtain­

ed in 6 patients. Migration anomalies were diagnosed

on the basis of characteristic morphology of the af­

fected brain on MR or CT.

Results

The clinical and radiologic findings of eleven pa­

tients are presented in Table 1. The neuronal migra­

tion anomalies in 11 patients included one with

lissencephaly. 9 with schizencephaly (2 with open lip

type and 7 with closed lip typeJ, and one with isolated

heterotopia. In one patient with lissencephaly. MR

demonstrated a figure of 8 appearance with a shallow

sylvian fissure caused by lack of opercularization (Fig.

1). The cortex was thick and white matter was

decreased in volume. The gray-white matter interface

was smooth due to the lack of white matter inter­

digitation . This patient also had persistent wide

이 논문은 1 990년 11 월 1 4일 접수하여 1991 년 3월 30일에 채택되었음

Received November 14. accepted March 30. 1991

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Journal of Korean Radiological Society 199 1; 27(3) 323-328

Table L Summary of Patients Data

Case Age (year) Presenting Symptoms MR diagnosis

No. I Sex

1. 5 /l 2/F seizure. la rge head agyria/pachygyria complex. colpocepha ly

2 11M developmental delay. abnormal face & ha ir schizencephaly. closed lip type. right

3 l lF left motor weakness schizencephaly. closed lip type. right

4. 41F seizure . development & m ental retardation schizencephaly. closed lip type. bilateral

5 101F seizure. m ental retardation. right schizencephaly ‘ closed lip type. left

motor weakness heterotopia

6 121F seizure. left hand paresis schizencephaly. closed lip type. right

7. 23/F facial palsy due to chronic mastoiditis isolated heterotopia. nodular form

incidental finding for migration disorder

8. 241F seizure. right hemiparesis schizencephaly. open lip type. left

9. 241M selzure schizenceph려y . closed lip type. right

heterotopia

10 351M selzure schizencephaly. closed lip type. bilateral 11. 42/M skull fracture by fall down. seizure. left schizencephaly. open lip type. right

motor weakness. mental retardation

lateral ventricles (colpocephaly). Nine patients with

schizencephaly had unilateral (7/9) (Fig. 2 .. Fig. 3b .)

or bilateral clefts (2/9) (Fig. 3a. ) that were lined by

gray matter. The clefts were commonly seen in the

parietal (parasylvian region) and temporal areas

Associated anomalies included absent septum

pellucidum (3/9) (Fig. 2.) and heterotopias (2/9).

Hydrocephalus was commonly seen associated

with an open form (Fig. 2.)

Heterotopias were seen in 3 patients. one with

isolated hete rotopia (Fig . 4.) and others with

associated schizencephaly (Fig . 2 .. 3. ).

Discussion

1 4

The process ofneuroblast formation begins at ap­

proximately 6 gestational weeks (3 . 4. 9. 29). First

wave of neuroblast formed in the germinal matrix

migrates through the white matter along ependymo­

glial process that stretches from the ventricular wall

through the white matter to the forming cortex. Such

peripheral migration along the glial guide is

designated radial migration and is most active dur­

ing the 3rd to 5th gestational months but continues

until approximately 5 months postnatally (1-4. 9. 29)

At this point. they differentiate further grow into ax­

ons and dendrites. and develop synaptic contacts

with other neurons . By the 6th month of gestation.

a 6 layered n eocortex is formed (4. 26).

Fig. L Lissencephaly . 2000/40 ax­ial proton density image Large areas of agyria are observed in the both parietooccipital lobes with partial gyral formation in anterior frontal lobes suggesting pachygyria. which shows hourglass configuration of brain and shallow smooth surface. There are also loss of cortical gray-white matter inter­digitation and colpocephaly . Fig. 4. Isolated gray matter heterotopia. Nodular gray matter indents the left frontal hom oflateral ventricle and diverticulum like ventricular pr이ec­

tion is also seen . Adj~cent insular cortex is somewhat thickened .

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Hyun Sook Hong , et al : MR Imaging of Neuronal Migration Anomaly

a b

a b

Smaller waves of cell migration continue up to 25

weeks. Any insu1t to the brain during this period

results in a migration anomalies (2 , 7 , 25-27 , 30-32).

The common underlying feature of migration

anoma1 ies is an abnormal location of neurons both

within and outside the cortex.

ln general, the cortex is thickened by a large

disorganized layer of neurons whose migration has

been prematurely halted. Pathologically , both agyric

and pachygyric regions ofthe brain have a 41ayered

cortex composed of a molecular layer , outer cellular

layer , a sparse celllayer , and an inner cellular layer.

The subcorticallayer ofwhite matter is thin because

organization of the neurons , which subsequently

stimulates axonal growth , has not occurred.

The term agyria refers to an absence of cortical

gyri , usually focal and holohemispheric. ln fac t. most

agyric brains have at least small area of gyral forma­

tion (1, 2 , 13 , 14 , 19 , 20). The area of broad f1at

shallo \V gyri are referred to area of pachygyria. The

term lissencephaly is sometimes used as a synonym

Fig. 2. Open lipped schizencephaly a . Axial proton density MR image (2000/3 8) demonstrates CSF c1efts extending from the venticle to the sulci , lined with gray matter bands in left precentral region , and mild­Iy dilated ventricular system . b. Coronal T1 WI image (500/38) well delineates the CSF c1eft , com­municating cortical sulci with the latera l ventricle , and agenesis of septum pellucidum

Fig. 3. Two cases of c losed lip schizencephaly a. Axial MR image (20001112) shows a band of thick gray matter extending from the ventricle to the cortical surface in postcentral region bilaterally. b . Axial MR image (2000/40) shows unila teral c10sed lip schizencepha­ly with gray matter heterotopia in right periventricular region.

for holohemispheric agyria and at other times as a

more general term encompassing the

agyria/pachygyria complex (2 , 15) .

Lissencephaly can be div ided into 3 types. Type

1 is characterized by microcephaly and dysmorphic

facies usually associated with heritable syndromes

such as Miller-Dieker syndrome , Norm an-Roberts

syndrome , and the Neu-Laxova syndrome. Type II

usually lacks characteris tic fac ies but exhibits

macrocephaly , retina1 dysplasia , congenita1 muscular

dystrophy , and/or posterior fossa abnormalities. The

Walker-Wanburg and the cerebro-ocular-muscular

syndrome are associated with type II. Type III is

heritable isolated lissencephaly a nd cerebro­

cerebellar lissencepha1y. Type III patients have the

best prognosis a nd longest suπival (2 , 3 , 7) . Our case

had no associated syndromes and abnormal fac e , so

probably type III.

The clinical features are seizure , developmental

delay , or mental retardation with the degree of severi­

ty related to the amount of abnormal cortex (25 , 27 ,

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Journal of Korean Radiological Society 1991; 27 (3) 323-328

31). MR exquisitely demonstrates the abnormal a r­

chitecture . MR shows the cortical convolutions and

gray-white m atter interface are smoother than nor

m a l a nd the s ubcortical white matter is thinned . The

insulae are exposed and the middle cerebral a rte ries

course superficially a long a shallow sylvian groove

No sylvian triangle is present (7. 8). A small bra in

stem is ofte n observed and may re f1ect lack of

development of the corticospinal tracts and subcor­

tical association fibers. Secondary findings of

lissencephaly include mild dilatation of the lateral

ventric1es with focally greater enlargement of the

atria and occipital horns (colpocephaly) (32) ..

The term schizencephaly has been used to

designate the presence of clefts which extend through

the entire cross section of the cerebral hemisphere

(1 . 7 . 22.24) . There are 2 forms. In the classic open

lip type. the cleft extends from the cortex to the ven­

tric les with gray matter lining. and CSF is interpos­

ed between the gray matter layers. The c10sed lip type

is differentiated from the open form by the fusion of

the opposing gray matter layers with exc1usion of the

interposed CSF spaces. A ventricular diverticulum of

varyng size is found at the base of the gray matter

columns (2. 5). At the margin of these clefts. the pial

covering of brain and the ependymal lining of ven

t ric le come to lie ex tremely c10se to each other a nd

m a y fuse togeth er. produc ing marginal pial­

ependymal seams . .The cause is failure of forma tion

of a segment of the germinal m atrix or segmental

failure of neurona l migration (2 . 3. 7. 17 ‘ 18). A1ter­

natively . they may represent secondary destruction

of the cerebral wall early in th e development. so a

spectrum of encepha loc1astic disorders (1. 10. 12. 26.

31. 33). The clinical features inc1ude seizure. m en­

tal retardation. a bnormal motor function. a nd

microcephaly . which is presumably realted to the

amount of brain tissue involved (1. 3).

MR is partic ularly s e nsitive in d etect ing

schizencephaly ‘ recognizing the presence of gray

m atte r lining the c1efts . which is critical to

distinguishing the disease from porencephaly. Our

cases of schizencephaly had common location in the

region of pre and post central gyr i. Heterotopias a re

frequent in both the walls of the lesions and the walls

of th e ven tric1es. Polymicrogyria or a bsence of sep

tum pellucidum is frequently observed. It is impor­

tant to understa nd that narrow c1efts can be identified

in only one imaging plane and be missed in anothe r

planes. In patients with horizontal c1efts. the abnor­

m a li ty would have been missed or misdiagnosed if

the coronal images were not obtained. Similarly. ver­

tically oriented narrow clefts can be missed if only

coronaJ images are obtained. We believe that MR

should be performed at least in 2 planes in order to

avoid such mistakes.

Unilateral megalencephaly is a rare anomaly of the

brain characterized by the early onset of intractable

seizures. hemiplegia. and severe developmental

delay. There is a marked overgrowth of part or a ll of

a cerebral hemisphere with defects in cell migra tion

in the affected a rea. In our cases. this anomly was

not found.

Gray matter heterotopias are a collection of nerve

cells in a bnormallocations as a result of arrest of their

radial migration. improper formation. or destruction

of the radiaJ glial fibers (1. 15) . Heterotopia has been

categorized in 2 forms (11. 15. 16. 2 1. 22. 29). The

subependymal nodular form is usually bilateral and

symmetrical wi th a predilection for the posterior a nd

anterior horns of the lateral ventric1es. The lamina r

form is an isla nd of cortical neurons oriented a long

their migrating path from the ventric1es to the cor­

tical gray matter. but which may be totally surround­

ed by white matter or bridge between the ependymal

surface a nd the cortica l gray matter. The lamina r

form is less common than nodula r form. Heterotopia

m ay occur as an IS이ated derangem ent or in associa­

tion with other more obvious migrational distur­

ba n ces such as pachygy ria. a nd agyr ia ‘

schizencephaly. When heterotopia occurs as a n

IS이ated entity. these children may be c1 inically

asymptomatic (case 7). When symptomatic. they

usually present with seizure (5. 6. 18. 22. 29).

Children with isolated heterotopia ha ve the best pro­

gnosis and longest surviva l. When heterotopia is

associated with other developm en tal anomalies. a

m yriad of clinical presentations are possible. On MR.

heterotopia is easily recognized as isointense foci with

gray matter in the corona radiata or subependymal

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Hyun Sook Hong , et al : MR Imaging of Neuronal Migration Anomaly

region (Fig. 4.) . They are much more read iJy identified

on MR than CT scan

Polymicrogyria (PMG) is an anomaly characteriz­

ed by excessive cerebral convolutions. increased cor­

tica l thickness and abnormal cortical histology. Since

the sulci πay not reach the surface of the brain . the

area ofpolymicrogyria resembles pachygyria. So the

diagnosis of polymicrogyria usually re quires

microscopic examintion. This is a pote ntial pitfall in

imaging diagnosis .

Conclusion

Migration anomalies are rare congenital m a lforma ­

tions and include a broad spectrum of anomalies

Minor disturbance s u c h as gray m atter heterotopia

is more common and may be clinically s iJe n t. We

retrospectively reviewed brain MR imaging of eleven

patients with migra tion anomalies (one with

lisse ncephaly. 9 with schize nce pha ly. a nd one with

isolated h eterotopia) . These patients presented with

a variety of symptoms. m ost commonly seizure.

d e layed development. and a bnormal motor skills.

MR clearly demonstrated the gray-white matter

differentiation a nd excellent anatomic detail. leading

to a correct diagnosis in a ll cases.

The results of our study s upport that MR appears

to be th e imaging method of choice for diagnosing

migration anomalies a nd the primary screening

m ethod for infants or ch iJdren who have seizure/and

d elayed developmen t.

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신경세포 이주 이상의 자기 공명 영상 소견

순천향대 학교 의과대학 방사선과학교실

홍현숙·최은완 ·김대호·정무찬·권귀향·깅기정

신경 세 포의 이주 이상(migrati on anomaly)은 드문 선천성 질환으로 배령 3-5개월 사이의 신경세포의 손상으로 일

어나며 여기에는 무뇌회/뇌회 비대 (Agyrial pachygyria) , 다왜소 뇌회증(polymicrogyria) ， 일측성 거뇌증(uni l ateral

megalencephaly) 및 이소성 회백절(gray matter heterotopia) 퉁이 포항된 다. 저자들은 최근 11예의 이 주 이상환자

(9 with schizencephaly, 1 with lissencephaly , and 1 with isolated heterotopia)를 경험하였기에 그 임상적 소견과

자기 공명 영상 소견을 문헌 고찰과 함께 보고하는 바이다

환자들은 다양한 임상 소견을 가졌으며 대개 경련발작， 발육 지연， 운동 장애 동의 소견을 보였고， 이러한 임상소

견은 뇌의 병소와 밀접한 연관성을 갖는 것으로 생각되었다.

자기 공명 영상은 뇌의 해부학적 구조를 보는데 우수하고， 여러면의 촬영을 할 수 있으며， 두개골에 의한 인공물

(Artifact)이 없어서 신경세포 이주 이상의 진단에 우수한 방법으로 생각된다.

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