대 한 방 사 선 의 학회 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

patients ranged in age from 5 months to 42 years with Introduction a mean of 16 years. The mean age was skewed by 2 patients with who were 35 and 42 Abnormalities of neuronal migration Sl re years old. characterized by anectopic location of in the MR was performed with a 0:2T permanent type (1-9). This broad group of anomalies (Hidachi PRP 20). Slice thickness was 5mm with a includes agyria. . schizencephaly. 2.5mm interslice gap or 7.5mm thickness. Spin echo unilateral . and gray matter axial images were obtained. including Tl weighted hcterotopia. Patients with this anomaly present images (TIWI) with a repetition time (TR) of clinically with a variety of symptoms which are pro­ 400-500ms and echo time (TE) of 25-40ms. in­ portional to the extent of the involved. These termediate images of TR/TE 2000/38. and T2 abnormalities have been characterized pathologically weighted images (T2Wl) with a TR/TE of 2000/110. in vivo by sonography and CT scan (2. 3. 10-14. Occasionally. sagittal and coronal images were ob­

15-21). tained. Gd-DTPA enhanced Tl WI were 려 so obtain­ MR appears to be an imaging technique of choice ed in 6 patients. Migration anomalies were diagnosed in evaluating these anomalies because it is capable on the basis of characteristic morphology of the af­ of exceptionally good differentiation between gray fected brain on MR or CT. and . high contrast resolution. m비 tiplan와 display of the anatomy. and lack of Results overlying bone artifact (1. 22-24). The purpose of this paper is to describe the MR fin­ The clinical and radiologic findings of eleven pa­ dings of neuronal migration anomaly. tients are presented in Table 1. The neuronal migra­ tion anomalies in 11 patients included one with Subjects and Methods . 9 with schizencephaly (2 with open lip type and 7 with closed lip typeJ, and one with isolated Eleven patients with neuronal migration heterotopia. In one patient with lissencephaly. MR anomalies were examined with MR (10 patients) and demonstrated a figure of 8 appearance with a shallow CT (one patient) from May 1989 to September 1990 sylvian fissure caused by lack of opercularization (Fig. because of . mental retardation. developmen­ 1). The cortex was thick and white matter was tal delay. enlarged head. and motor weakness. The decreased in volume. The gray-white matter interface

Index Words: Brain. abnormalities. 13. 14. was smooth due to the lack of white matter inter­ digitation. This patient also had persistent wide Brain‘ MR imagings. 13 ‘ 1214

이 논문은 1 990 년 11 월 1 4 일 접수하여 1991 년 3 월 30 일 에 채택되었 음 Received November 14. accepted March 30. 1991 - 323- Journal of Korean Radiological Society 1991; 27(3) 323-328

Table L Summary of Patients Data

Case Age (year) Presenting Symptoms MR diagnosis No. I Sex

1. 5/l2/F seizure. large head agyria/pachygyria complex. 2 11M developmental delay. abnormal face & hair 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 schizencephaly. open lip type. left 9. 241M selzure schizence ph려 y . 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

(colpocephaly). Nine patients with The process ofneuroblast formation begins at ap­ schizencephaly had unilateral (7/9) (Fig. 2 .. Fig. 3b.) proximately 6 gestational weeks (3. 4. 9. 29). First or bilateral clefts (2/9) (Fig. 3a.) that were lined by wave of formed in the germinal matrix gray matter. The clefts were commonly seen in the migrates through the white matter along ependymo­ parietal (parasylvian region) and temporal areas glial process that stretches from the ventricular wall Associated anomalies included absent septum through the white matter to the forming cortex. Such pellucidum (3/9) (Fig. 2.) and heterotopias (2/9). peripheral migration along the glial guide is was commonly seen associated designated radial migration and is most active dur­ with an open form (Fig. 2.) ing the 3rd to 5th gestational months but continues Heterotopias were seen in 3 patients. one with until approximately 5 months postnatally (1-4. 9. 29) isolated hete rotopia (Fig . 4.) and others with At this point. they differentiate further grow into ax­ associated schizencephaly (Fig. 2 .. 3.). ons and dendrites. and develop synaptic contacts with other neurons. By the 6th month of gestation. Discussion a 6 layered n eocortex is formed (4. 26).

Fig. L Lissencephaly. 2000/40 ax­ ial 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 inter­ digitation and colpocephaly. Fig. 4. Isolated gray matter heterotopia. Nodular gray matter indents the left 1 4 frontal hom oflateral ventricle and diverticulum like ventricular pr이 ec­ tion is also seen. Adj~cent insular cortex is somewhat thickened. - 324- Hyun Sook Hong , et al : MR Imaging of Neuronal Migration Anomaly

Fig. 2. Open lipped schizencephaly a . Axial proton density MR image (2000/3 8) demonstrates CSF c1 efts extending from the venticle to the sulci, lined with gray matter bands in left precentral region, and mild­ Iy dilated . b. Coronal T1 WI image (500/38) well delineates the CSF c1eft, com­ municating cortical sulci with the lateral ventricle, and agenesis of septum pellucidum

a b

Fig. 3. Two cases of closed 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 schizencepha­ ly with gray matter heterotopia in right periventricular region.

a b

Smaller waves of cell migration continue up to 25 for holohemispheric agyria and at other times as a weeks. Any insu1t to the brain during this period more general term encompassing the results in a migration anomalies (2 , 7 , 25-27, 30-32). agyria/pachygyria complex (2 , 15). The common underlying feature of migration Lissencephaly can be divided into 3 types. Type anoma1 ies is an abnormal location of neurons both 1 is characterized by and dysmorphic within and outside the cortex. facies usually associated with heritable syndromes ln general, the cortex is thickened by a large such as Miller-Dieker syndrome, Norm an-Roberts disorganized layer of neurons whose migration has syndrome, and the Neu-Laxova syndrome. Type II been prematurely halted. Pathologically, both agyric usually lacks characteris tic facies but exhibits and pachygyric regions ofthe brain have a 41ayered , retina1 dysplasia, congenita1 muscular cortex composed of a molecular layer, outer cellular dystrophy, and/or posterior fossa abnormalities. The layer, a sparse celllayer, and an inner cellular layer. Walker-Wanburg and the cerebro-ocular-muscular The subcorticallayer ofwhite matter is thin because syndrome are associated with type II. Type III is organization of the neurons, which subsequently heritable isolated lissencephaly a nd cerebro­ stimulates axonal growth, has not occurred. cerebellar lissencepha1 y. Type III patients have the

The term agyria refers to an absence of cortical best prognosis a nd longest suπival (2 , 3 , 7). Our case gyri, usually focal and holohemispheric. ln fact. most had no associated syndromes and abnormal face , so agyric have at least small area of gyral forma­ probably type III. tion (1, 2 , 13, 14, 19, 20). The area of broad f1 at The clinical features are seizure, developmental shallo\V gyri are referred to area of pachygyria. The delay, or mental retardation with the degree of severi­ term lissencephaly is sometimes used as a synonym ty related to the amount of abnormal cortex (25, 27 ,

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31). MR exquisitely demonstrates the abnormal a r­ of th e ventric1 es. or a bsence of sep chitecture. MR shows the cortical convolutions and tum pellucidum is frequently observed. It is impor­ gray-white m atter interface are smoother than nor tant to understa nd that narrow c1efts can be identified m a l a nd the s ubcortical white matter is thinned . The in only one imaging plane and be missed in anothe r insulae are exposed and the middle cerebral a rteries planes. In patients with horizontal c1 efts. the abnor­ course superficially a long a shallow sylvian groove m a li ty would have been missed or misdiagnosed if No sylvian triangle is present (7. 8). A small bra in the coronal images were not obtained. Similarly. ver­ stem is ofte n observed and may ref1 ect lack of tically oriented narrow clefts can be missed if only development of the corticospinal tracts and subcor­ coronaJ images are obtained. We believe that MR tical association fibers. Secondary findings of should be performed at least in 2 planes in order to lissencephaly include mild dilatation of the lateral avoid such mistakes. ventric1es with fo cally greater enlargement of the Unilateral megalencephaly is a rare anomaly of the atria and occipital horns (colpocephaly) (32) .. brain characterized by the early onset of intractable The term schizencephaly has been used to . hemiplegia. and severe developmental designate the presence of clefts which extend through delay. There is a marked overgrowth of part or a ll of the entire cross section of the a cerebral hemisphere with defects in cell migra tion (1 . 7. 22.24). There are 2 forms. In the classic open in the affected a rea. In our cases. this anomly was lip type. the cleft extends from the cortex to the ven­ not found. tricles with gray matter lining. and CSF is interpos­ Gray matter heterotopias are a coll ection of nerve ed between the gray matter layers. The c10sed lip type cells in a bnormallocations as a result of arrest of their is differentiated from the open form by the fusion of radial migration. improper formation. or destruction the opposing gray matter layers with exc1 usion of the of the radiaJ glial fibers (1. 15). Heterotopia has been interposed CSF spaces. A ventricular diverticulum of categorized in 2 forms (11. 15. 16. 2 1. 22. 29). The varyng size is found at the base of the gray matter subependymal nodular form is usually bilateral and columns (2. 5). At the margin of these clefts. the pial symmetrical with a predilection for the posterior a nd covering of brain and the ependymal lining of ven anterior horns of the lateral ventric1es. The lamina r tricle come to lie extremely c10se to each other a nd form is an isla nd of cortical neurons oriented a long m a y fuse togeth er. producing marginal pial­ their migrating path from the ventric1 es to the cor­ ependymal seams . .The cause is failure of forma tion tical gray matter. but which may be totally surround­ of a segment of the germinal m atrix or segmental ed by white matter or bridge between the ependymal failure of neurona l migration (2 . 3. 7. 17‘ 18). A1ter­ surface a nd the cortica l gray matter. The lamina r natively. they may represent secondary destruction form is less common than nodula r form. Heterotopia of the cerebral wall early in th e development. so a m ay occur as an IS 이 a te d derangem ent or in associa­ spectrum of encepha loc1 astic disorders (1. 10. 12. 26. tion with other more obvious migrational distur­

31. 33). The clinical features inc1 ude seizure. m en­ ba n ces such as pachygyria. a nd agyria ‘ tal retardation. a bnormal motor function. a nd schizencephaly. When heterotopia occurs as a n microcephaly. which is presumably realted to the IS이 ate d entity. these children may be c1 inically amount of brain tissue involved (1. 3). asymptomatic (case 7). When symptomatic. they MR is partic ularly s e nsitive in d etecting usually present with seizure (5. 6. 18. 22. 29). schizencephaly‘ recognizing the presence of gray Children with isolated heterotopia ha ve the best pro­ m atter lining the c1 efts. which is critical to gnosis and longest survival. When heterotopia is distinguishing the disease from . Our associated with other developm en tal anomalies. a cases of schizencephaly had common location in the m yriad of clinical presentations are possible. On MR. region of pre and post central gyri. Heterotopias a re heterotopia is easily recognized as isointense foci with frequent in both the walls of the lesions and the walls gray matter in the corona radiata or subependymal

- 326 - Hyun Sook Hong, et al : MR Imaging of Neuronal Migration Anomaly region (Fig. 4.). They are much more readiJy identified 5. Pollei SR. Boyer RS. Crawford S et al. Disorders of on MR than CT scan Migration and sulcation. Seminars in US. CT a nd Polymicrogyria (PMG) is an anomaly c haracteriz­ MR. 1988‘ 9(3):231-246 ed by excessive cerebral convolutions. increased cor­ 6. Osborn RE. Byrd SE. Naidich TP et a l. MR imaging tical thickness and abnormal cortical histology. Since of Neuronal migrational disorders. AJNR. 1988: 9 ‘ 1101-1106 the sulci πay not reach the surface of the brain. the 7. Byrd SE. Naidich TP. Common congenital brain area ofpolymicrogyria resembles pachygyria. So the a nomalies. RCNA. 1988; 26(4):755-722 diagnosis of polymicrogyria usually re quires 8. Naidich TP. Zimmermann RA. Common congenital microscopic examintion. This is a pote ntial pitfall in m alformation of the brain. ln Bra ndt-Zawadzki M. imaging diagnosis. Norman D (eds): Magnetic resonance Imaging of the central . 13 1-150. 1987. Raven Conclusion Press. New York. 1987 9. Larroche TC. Malformations of the nervous system ‘ Migration anomalies are rare congenital m a lforma ­ In Adams JH. Orsellis JAN. Duchen LW (eds ). tions and include a broad spectrum of anomalies Neuropathology. 4th ED. 385-450. 1984. John Witey Minor disturbance s u c h as gray m atter heterotopia a nd Sons ‘ New York is more common and may be clinically s iJ e n t. We 10. Klingensmith WC III . Cloffi-Ragan DT. retrospectively reviewed brain MR imaging of eleven Schizencephaly: Diagnosis and progressive in u tero. Radiology. 1986: 159:617-618 patie nts with migra tion anomalies (one with 1 1. Di Pietro MA . Brody BA. Kuban K et a l. lisse ncephaly. 9 with schize nce phaly. a nd one with Sc hizencepha ly: Rare cerebral m alformation isolated h eterotopia). These patients presented with demonstrated by sonograph y. AJNR. 1984: a variety of symptoms. m ost commonly seizure. 5 ‘ 196-198 delayed development. and a bnormal motor skills. 12. 임효 근 ， 주 인욱 ， 배상 훈 둥 : Sc hiz e n ce ph a l y 의 전산화 MR clearly demonstrated the gray-white matter 단 층 촬영 및 자기공명영상 소견. 대한방사선의학회 differentiation a nd excellent anatomic detail. leading 지 . 1990; 26(2) : 275-278 to a correct diagnosis in a ll cases. 13. Motte J ‘ Gomes H. Morville P et a l. Sonographic The results of our study s upport that MR appears diagnos is of lissencephaly. Pediatr. Radiol. 1987: to be th e imaging method of choice for diagnosing 17:362-364 migration anomalies a nd the primary screening 14. Ramirez RE. Sonographic re cognition of m ethod for infants or ch iJdren who have seizure/and lissencephaly (Agyria). AJNR. 1984: 5:830-831 d elayed development. 15. Bairaman D. DiChiro G. Theodore WH et al. MR im­ aging and positron emission tomography of cortical heterotopia. J . comput. Assist Tomogr. 1985; REFERENCES 9(6): 11 37 -1139 1. Barkovich AJ. Chuang SH. Norma n D. MR of 16. Deeb ZL. Rothfus WE. Maroon J C. MR imaging of neuronal migration a noma li es. AJNR. 1987; heterotopic gray m atter. J Comput Assist. Tomogr.

8 : 1009-1017 1985 ‘ 9(6):1140-1141 2. Zimmerman RA. Bilaniuk L T. Grossmann RI. Com­ 17. Dob y n s WB. McCluggage CW. Computed puted tomography in migratory disorders ofhuman tomographic a ppearance of Lissencephaly syn­ brain development. Neuroradiology 1983; 25:257- dromes. AJNR. 1985; 6:545-550 263 18. Byrd SE. Osborn RE. Bohan TD et a l. The CT a nd 3. Miller GM. Stears JC. Guggenheim MA et a l. MR evaluation ofmigrational disorders ofthe brain.

Schizencephaly: A clinical a nd CT study. Part 11. S c hizencephaly ‘ h eterotopia a nd 1984: 34:997-1001 polymicrogyria . Pediatr. Radiol. 1989: 19:219-222 4. Rakic P. Neuronal migration a nd contact guidance 19. Byrd SE. Osborn RE. Bohan TD et a l. The CT and

in the primate telencephalon. Post Grad Med. J MR evaJuation ofmigrationaJ disorders ofthe brain ‘ (suppl 1) 1978; 54:25-37 Part 1. Lissencepha Jy and pachygyria. Pediatr. - 327 Journal of Korean Radiological Societv 1991; 27(3) 323-328

Radiol. 1989: 19:151-156 pellucidum: A usefu1 sign in the diagnosis of con­ 20. Byrd SE. Bohan TD. Osborn RE et a l. The CT and genita1 brain ma1formation. AJNR. 1988; MR evaluation of Lissencephaly. AJNR. 1988: 9:1107-1114 9 :923-927 29. Meencke HJ. Janz D. The significance of 2 1. Mikhae1 MA. Mutter AG. Ma1formation of the microdysgenesis in primary generalized cerebra1 cortex with heterotopia of the gray matter. An answer to the considerations of Lyon and J . comput Assist Tomogr. 1978; 2:291-296 Gastaut. Epilepsia. 1985; 26(4):368-371 22. Smith AS. Weinstein MA. Quencer RM et al. Associa­ 30. A1varez LA. Yamamoto T. Wong B et a l. Mil1er­ tion of heterotopic gray matter with seizures: MR im­ Dieker syndrome: a disorder affecting pathways of aging. Work in progress. Radio10gy. 1988; neurona1 migration. Neuro10gy. 1986; 36:489-493 168:195-198 31. Grummet ML. Ba1e JF J r. Brain abnormalities in in­ 23. McMurdo SK. Moore SG. Brant-Zawadiski M et a1 fant with Potter syndrome. Neuro10gy. 1981; MR imaging of Intracrania1 tuberous s c1 erosis 31:1571-1573 AJNR. 1987; 8:77-82 32. Herskowitz J. Rosman NP. Whee1er CB. Co1pocepha- 24. Barkovich AJ. Norman D. MR imaging of schizen­ 1y: Clinica1 and radio10gic and pathogenetic aspects cepha1y. AJNR. 1988; 9:297-302 neuro10gy. 1985; 1594-1598 25. Van All en M. C1arren SK. A spectrum of gyra1 ab­ 33. Barkovich AJ. Abnormal vascular drainage in normalities in Mil1er-Dieker (Lissencepha1y) syn­ anomalies of neurona1 migration. AJNR. 1988;

drome. J Pediatr. 1983; 102:559-564 9 ’ 1107-1114 26. Ravbaud C. Destructive 1esions of the brain 34. Fitz CR. Harwood-Nash DC. Bolat DW. The Neuroradio10gy. 1988; 25:265-291 radiographic features of unilatera1 megalencepha- 27. Dobyns WB. Stratton RF. Greenberg F. Syndromes 1y. Neuroradio10gy. 1973; 15: 145-148 with lissencepha1y 1: Mil1er- Dieker and Norman­ 35. Towsend JJ. Nie1sen SI. Maimud N. Unilatera1 Roberts syndromes a nd iso1ated lissencepha1y. Am m ega1encepha1y: Harmatoma or Neop1asm? J Med Genet. 1984; 18:509-526 Neuro10gy. 1975; 25:448-453 28. Barkovich AJ. Norman D. Absence of the septum

〈국문요약 〉 신경세포 이주 이상의 자기 공명 영상 소견 순천향 대 학교 의과대학 방사선과학교실 홍현숙·최은완 ·김 대호·정무찬·권귀향·깅기정 신경 세 포의 이주 이상 (migrati o n anomaly) 은 드문 선천성 질환으로 배령 3-5 개월 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. 저자 들은 최근 11 예의 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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