皮质发育畸形大鼠皮质神经元AIS的可塑性研究
|
摘要
目的研究皮质发育畸形(MCD)仔鼠与正常仔鼠的生长发育差异,动态监测层特异性标志物Map1b和AIS的标记物AnkG在MCD大鼠皮质中的表达变化,揭示MCD大鼠皮质AIS区的可塑性改变,为深入探讨AIS对MCD大鼠模型癫痫易感的意义提供实验室依据。
方法在SD大鼠胚胎17天时,向孕鼠腹腔注射卡莫司汀(BCMU),建立皮质发育畸形仔鼠模型,对照组在相同时间注射10%葡萄糖溶液。选择出生当天(P0),出生后7天(P7),14天(P14),28天(P28)和56天(P56)作为观察时间点,分别在各时间点选取对照组和MCD组仔鼠进行体重,脑湿重,身长的测量。在各时间点每组随机选取6只仔鼠用于制备石蜡切片和冰冻切片,采用HE染色方法观察两组仔鼠皮质的形态改变,免疫组织化学染色方法观察Maplb在两组皮质内的表达差异,并验证MCD模型是否成功,应用免疫荧光染色方法观察AnkG在两组皮质内的表达变化。
结果两组仔鼠的体重在PO期无显著差异(P>0.05),从P7后开始,之后的各时间点体重差异有统计学意义(P<0.05)；两组仔鼠的脑湿重在PO和P7无显著差异(P>0.05),从P14开始,之后的各时间点差异有统计学意义(P<0.05)；两组仔鼠身长在各时间点均无显著差异(P>0.05)。Map1b在对照组仔鼠颞叶皮质中主要表达在Ⅱ,Ⅲ,Ⅴ层,在各时间点的表达模式无明显变化,Map1b在MCD组仔鼠颞叶皮质中表达在Ⅱ,Ⅲ,Ⅳ层。在MCD组仔鼠皮质中,AnkG阳性细胞形态与对照组存在显著差异,AIS形态正常化时间晚于对照组,AnkG阳性区域所代表的AIS长度在PO时与对照组无显著差异(P>0.05),从P7开始,之后的各时间点的AIS长度均短于对照组(P<0.05)。
结论Map1b在MCD组仔鼠皮质中的表达位置由正常的ⅡⅢⅤ层转移到Ⅱ ⅢⅣ层对应的位置,提示在MCD大鼠皮质中,Map1b所标记的阳性细胞发生迁移异常；MCD组仔鼠脑皮质AIS的长度在出生一周后有所缩短,形态表现为螺旋状或锯齿状弯曲,形态正常化的时间延迟,提示MCD大鼠模型皮质神经元AIS发生可塑性改变。
Object To study the development differences between the malformation of cortical development (MCD) and normal Sprahue Dawley (SD) rats. To observe the expression changes of layer-specific markers Maplb in MCD rats' cortex. To investigate the expression of AnkG in MCD rats cortical AIS area, reveals the morphological changes of AIS area in the MCD rats'cortex, and then explore the significance to epilepsy susceptibility of MCD animal model.
Methods The experimental group rats were induced cortical malformation with BCMU by intraperitoneal injection at the17th day of pregnantce. The control group were injected with10%glucose solution at the same time. Select the day of birth (P0),7days after birth (P7),14days (P14),28days (P28) and56days (P56) as the observation time, then we selected two groups with the same numbers of pups at each observation time, taking the weight, the brain wet weight, and height measurement. We randomly selected six pups from each group at each observation time for the preparation of paraffin sections and frozen sections. Observation of morphological changes of the two groups'cortex by HE staining, immunohistochemical staining was used to observ MAP1B expression in the cortex, and verify the success of the MCD model, immunofluorescence staining method used to observe the AnkG expression differences in the two sets of cortex.
Results There were no significant difference (P>0.05) in weight between two groups at P0, the difference was significant starting from P7(P<0.05); There were no significant difference (P>0.05) in brain wet weight between two groups at PO and P7(P>0.05), it was significant starting from the time of P14(P<0.05); There were no significant difference (P>0.05) in height at any observation time. MAP1B expressed in Ⅱ, Ⅲ, Ⅴ layer in the temporal cortex of control group, no significant expression changes happened at any observation time, MAP1B expressed in Ⅱ, Ⅲ, Ⅳ layer in MCD group. There were significant differences in morphology of AnkG+cell between two groups, the normalization of AIS morphology in MCD group was later than that in the control group. The length of the AnkG+cell in MCD group were shorter than that in the control group from the time of P7(P<0.05).
Conclusions The weight development of MCD group lagged far behind that in the control group from the first week after birth; The brain wet weight development of MCD group lagged far behind that in the control group from the second week after birth; There was no significant difference in height between two groups; Maplb+cell expressed in Ⅱ Ⅲ Ⅴ layer in the nomal group; The expression pattern of Maplb changed from different area in the MCD group, it expressed in Ⅱ, Ⅲ, Ⅳ layer in the temporal cortex; There were significant differences in the morphology of AIS between two group, There were significant differences in the length of AIS between two group from the first week after birth:the length of AIS is shortened in the MCD cortex, the normalization of AIS morphology delayed.
方法在SD大鼠胚胎17天时,向孕鼠腹腔注射卡莫司汀(BCMU),建立皮质发育畸形仔鼠模型,对照组在相同时间注射10%葡萄糖溶液。选择出生当天(P0),出生后7天(P7),14天(P14),28天(P28)和56天(P56)作为观察时间点,分别在各时间点选取对照组和MCD组仔鼠进行体重,脑湿重,身长的测量。在各时间点每组随机选取6只仔鼠用于制备石蜡切片和冰冻切片,采用HE染色方法观察两组仔鼠皮质的形态改变,免疫组织化学染色方法观察Maplb在两组皮质内的表达差异,并验证MCD模型是否成功,应用免疫荧光染色方法观察AnkG在两组皮质内的表达变化。
结果两组仔鼠的体重在PO期无显著差异(P>0.05),从P7后开始,之后的各时间点体重差异有统计学意义(P<0.05)；两组仔鼠的脑湿重在PO和P7无显著差异(P>0.05),从P14开始,之后的各时间点差异有统计学意义(P<0.05)；两组仔鼠身长在各时间点均无显著差异(P>0.05)。Map1b在对照组仔鼠颞叶皮质中主要表达在Ⅱ,Ⅲ,Ⅴ层,在各时间点的表达模式无明显变化,Map1b在MCD组仔鼠颞叶皮质中表达在Ⅱ,Ⅲ,Ⅳ层。在MCD组仔鼠皮质中,AnkG阳性细胞形态与对照组存在显著差异,AIS形态正常化时间晚于对照组,AnkG阳性区域所代表的AIS长度在PO时与对照组无显著差异(P>0.05),从P7开始,之后的各时间点的AIS长度均短于对照组(P<0.05)。
结论Map1b在MCD组仔鼠皮质中的表达位置由正常的ⅡⅢⅤ层转移到Ⅱ ⅢⅣ层对应的位置,提示在MCD大鼠皮质中,Map1b所标记的阳性细胞发生迁移异常；MCD组仔鼠脑皮质AIS的长度在出生一周后有所缩短,形态表现为螺旋状或锯齿状弯曲,形态正常化的时间延迟,提示MCD大鼠模型皮质神经元AIS发生可塑性改变。
Object To study the development differences between the malformation of cortical development (MCD) and normal Sprahue Dawley (SD) rats. To observe the expression changes of layer-specific markers Maplb in MCD rats' cortex. To investigate the expression of AnkG in MCD rats cortical AIS area, reveals the morphological changes of AIS area in the MCD rats'cortex, and then explore the significance to epilepsy susceptibility of MCD animal model.
Methods The experimental group rats were induced cortical malformation with BCMU by intraperitoneal injection at the17th day of pregnantce. The control group were injected with10%glucose solution at the same time. Select the day of birth (P0),7days after birth (P7),14days (P14),28days (P28) and56days (P56) as the observation time, then we selected two groups with the same numbers of pups at each observation time, taking the weight, the brain wet weight, and height measurement. We randomly selected six pups from each group at each observation time for the preparation of paraffin sections and frozen sections. Observation of morphological changes of the two groups'cortex by HE staining, immunohistochemical staining was used to observ MAP1B expression in the cortex, and verify the success of the MCD model, immunofluorescence staining method used to observe the AnkG expression differences in the two sets of cortex.
Results There were no significant difference (P>0.05) in weight between two groups at P0, the difference was significant starting from P7(P<0.05); There were no significant difference (P>0.05) in brain wet weight between two groups at PO and P7(P>0.05), it was significant starting from the time of P14(P<0.05); There were no significant difference (P>0.05) in height at any observation time. MAP1B expressed in Ⅱ, Ⅲ, Ⅴ layer in the temporal cortex of control group, no significant expression changes happened at any observation time, MAP1B expressed in Ⅱ, Ⅲ, Ⅳ layer in MCD group. There were significant differences in morphology of AnkG+cell between two groups, the normalization of AIS morphology in MCD group was later than that in the control group. The length of the AnkG+cell in MCD group were shorter than that in the control group from the time of P7(P<0.05).
Conclusions The weight development of MCD group lagged far behind that in the control group from the first week after birth; The brain wet weight development of MCD group lagged far behind that in the control group from the second week after birth; There was no significant difference in height between two groups; Maplb+cell expressed in Ⅱ Ⅲ Ⅴ layer in the nomal group; The expression pattern of Maplb changed from different area in the MCD group, it expressed in Ⅱ, Ⅲ, Ⅳ layer in the temporal cortex; There were significant differences in the morphology of AIS between two group, There were significant differences in the length of AIS between two group from the first week after birth:the length of AIS is shortened in the MCD cortex, the normalization of AIS morphology delayed.
引文
[1]KUZNIECKY R I. Magnetic resonance imaging in developmental disorders of the cerebral cortex [J]. Epilepsia,1994,35 Suppl 6(S44-56.
[2]MORONI R F, CIPELLETTI B, INVERARDI F, et al. Development of cortical malformations in BCNU-treated rat, model of cortical dysplasia [J]. Neuros-cience,2011,175(380-93.
[3]BENARDETE E A, KRIEGSTEIN A R. Increased excitability and decreased sensitivity to GAB A in an animal model of dysplastic cortex [J]. Epilepsia,2002, 43(9):970-82.
[4]WIMMER V C, REID C A, SO E Y, et al. Axon initial segment dysfunction in epilepsy [J]. The Journal of physiology,2010,588(Pt 11):1829-40.
[5]SUN X Z, TAKAHASHI S, FUKUI Y, et al. Neurogenesis of heterotopic gray matter in the brain of the microcephalic mouse [J]. Journal of neuroscience research,2001,66(6):1083-93.
[6]BATTAGLIA G, PAGLIARDINI S, SAGLIETTI L, et al. Neurogenesis in cerebral heterotopia induced in rats by prenatal methylazoxymethanol treatment [J]. Cerebral cortex,2003,13(7):736-48.
[7]POLUCH S, JULIANO S L. A normal radial glial scaffold is necessary for migration of interneurons during neocortical development [J]. Glia,2007,55(8): 822-30.
[8]WONG M. Animal models of focal cortical dysplasia and tuberous sclerosis complex:recent progress toward clinical applications [J]. Epilepsia,2009,50 Suppl 9(34-44.
[9]MORONI R F, INVERARDI F, REGONDI M C, et al. Expression of layer-specific markers in the adult neocortex of BCNU-Treated rat, a model of cortical dysplasia [J]. Neuroscience,2009,159(2):682-91.
[10]ZIMMER C, TIVERON M C, BODMER R, et al. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons [J]. Cerebral cortex,2004,14(12):1408-20.
[11]YONESHIMA H, YAMASAKI S, VOELKER C C, et al. Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices [J]. Neuroscience,2006,137(2):401-12.
[12]WATAKABE A, ICHINOHE N, OHSAWA S, et al. Comparative analysis of layer-specific genes in Mammalian neocortex [J]. Cerebral cortex,2007,17(8): 1918-33.
[13]FERRER I, BERNET E, SORIANO E, et al. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes [J]. Neuroscience,1990,39(2):451-8.
[14]SPREAFICO R, FRASSONI C, ARCELLI P, et al. In situ labeling of apoptotic cell death in the cerebral cortex and thalamus of rats during development [J]. The Journal of comparative neurology,1995,363(2):281-95.
[15]DALMAU I, VELA J M, GONZALEZ B, et al. Dynamics of microglia in the developing rat brain [J]. The Journal of comparative neurology,2003,458(2): 144-57.
[16]MORONI R F, INVERARDI F, REGONDI M C, et al. Altered spatial distribution of PV-cortical cells and dysmorphic neurons in the somatosensory cortex of BCNU-treated rat model of cortical dysplasia [J]. Epilepsia,2008, 49(5):872-87.
[17]GARBELLI R, MUNARI C, DE BIASI S, et al. Taylor's cortical dysplasia:a confocal and ultrastructural immunohistochemical study [J]. Brain pathology, 1999,9(3):445-61.
[18]SPREAFICO R, TASSI L, COLOMBO N, et al. Inhibitory circuits in human dysplastic tissue [J]. Epilepsia,2000,41 Suppl 6(S 168-73.
[19]CRINO P B, DUHAIME A C, BALTUCH G, et al. Differential expression of glutamate and GAB A-A receptor subunit mRNA in cortical dysplasia [J]. Neurology,2001,56(7):906-13.
[20]OGHLAKIAN R O, TILELLI C Q, HIREMATH G K, et al. Single injection of a low dose of pentylenetetrazole leads to epileptogenesis in an animal model of cortical dysplasia [J]. Epilepsia,2009,50(4):801-10.
[21]KELLINGHAUS C, MODDEL G, SHIGETO H, et al. Dissociation between in vitro and in vivo epileptogenicity in a rat model of cortical dysplasia [J]. Epile-ptic disorders:international epilepsy journal with videotape,2007,9(1):11-9.
[22]LONG L L, XIAO B, SONG Y M, et al. [Changes of expression of cation-chloride cotransporter genes in hippocampus of cortical dysplasia: experiment with rat] [J]. Zhonghua yi xue za zhi,2007,87(19):1351-4.
[23]NIETO M, MONUKI E S, TANG H, et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex [J]. The Journal of comparative neurology,2004,479(2):168-80.
[24]BRITANOVA O, DE JUAN ROMERO C, CHEUNG A, et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex [J]. Neuron,2008,57(3):378-92.
[25]SHEEN V L, FERLAND R J, NEAL J, et al. Neocortical neuronal arrangement in Miller Dieker syndrome [J]. Acta neuropathologica,2006,111(5):489-96.
[26]ARLOTTA P, MOLYNEAUX B J, CHEN J, et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo [J]. Neuron, 2005,45(2):207-21.
[27]HEVNER R F, SHI L, JUSTICE N, et al. Tbrl regulates differentiation of the preplate and layer 6 [J]. Neuron,2001,29(2):353-66.
[28]FERLAND R J, CHERRY T J, PREWARE P O, et al. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain [J]. The Journal of comparative neurology,2003,460(2):266-79.
[29]HEVNER R F, MIYASHITA-LIN E, RUBENSTEIN J L. Cortical and thalamic axon pathfinding defects in Tbrl, Gbx2, and Pax6 mutant mice:evidence that cortical and thalamic axons interact and guide each other [J]. The Journal of comparative neurology,2002,447(1):8-17.
[30]GUILLEMOT F, MOLNAR Z, TARABYKIN V, et al. Molecular mechanisms of cortical differentiation [J]. Eur J Neurosci,2006,23(4):857-68.
[31]LEONE D P, SRINIVASAN K, CHEN B, et al. The determination of projection neuron identity in the developing cerebral cortex [J]. Current opinion in neurobiology,2008,18(1):28-35.
[32]MATSUMOTO H, JIANG J Y, MITANI D, et al. Distribution and gene expression of cytoskeletal proteins in two-cell rat embryos and developmental arrest [J]. The Journal of experimental zoology,2002,293(7):641-8.
[33]LI S, JIN Z, KOIRALA S, et al. GPR56 regulates pial basement membrane integrity and cortical lamination [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(22):5817-26.
[34]OGAWA Y, RASBAND M N. The functional organization and assembly of the axon initial segment [J]. Current opinion in neurobiology,2008,18(3):307-13.
[35]RASBAND M N. The axon initial segment and the maintenance of neuronal polarity [J]. Nature reviews Neuroscience,2010,11(8):552-62.
[36]KOLE M H, ILSCHNER S U, KAMPA B M, et al. Action potential generation requires a high sodium channel density in the axon initial segment [J]. Nature neuroscience,2008,11(2):178-86.
[37]KOLE M H, LETZKUS J J, STUART G J. Axon initial segment Kvl channels control axonal action potential waveform and synaptic efficacy [J]. Neuron, 2007,55(4):633-47.
[38]GOLDBERG E M, CLARK B D, ZAGHA E, et al. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons [J]. Neuron,2008,58(3):387-400.
[39]NAUNDORF B, WOLF F, VOLGUSHEV M. Unique features of action potential initiation in cortical neurons [J]. Nature,2006,440(7087):1060-3.
[40]SCHAFER D P, JHA S, LIU F, et al. Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2009,29(42): 13242-54.
[41]KUBA H, OICHI Y, OHMORI H. Presynaptic activity regulates Na(+) channel distribution at the axon initial segment [J]. Nature,2010,465(7301):1075-8.
[42]GRUBB M S, BURRONE J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability [J]. Nature,2010,465(7301):1070-4.
[43]GRUNDEMANN J, HAUSSER M. Neuroscience:A plastic axonal hotspot [J]. Nature,2010,465(7301):1022-3.
[44]HINMAN J D, RASBAND M N, CARMICHAEL S T. Remodeling of the axon initial segment after focal cortical and white matter stroke [J]. Stroke; a journal of cerebral circulation,2013,44(1):182-9.
[45]WIMMER V C, REID C A, MITCHELL S, et al. Axon initial segment dysfunction in a mouse model of genetic epilepsy with febrile seizures plus [J]. The Journal of clinical investigation,2010,120(8):2661-71.
[46]THOMAS E A, HAWKINS R J, RICHARDS K L, et al. Heat opens axon initial segment sodium channels:a febrile seizure mechanism? [J]. Annals of neurology,2009,66(2):219-26.
[47]BLUMENFELD H, LAMPERT A, KLEIN J P, et al. Role of hippocampal sodium channel Navl.6 in kindling epileptogenesis [J]. Epilepsia,2009,50(1): 44-55.
[48]HUANG Z J, DI CRISTO G, ANGO F. Development of GABA innervation in the cerebral and cerebellar cortices [J]. Nature reviews Neuroscience,2007,8(9): 673-86.
[49]FAIREN A, VALVERDE F. A specialized type of neuron in the visual cortex of cat:a Golgi and electron microscope study of chandelier cells [J]. The Journal of comparative neurology,1980,194(4):761-79.
[50]DEFELIPE J. Chandelier cells and epilepsy [J]. Brain:a journal of neurology, 1999,122 (Pt10)(1807-22.
[1]KUZNIECKY R I. Magnetic resonance imaging in developmental disorders of the cerebral cortex [J]. Epilepsia,1994,35 Suppl 6(S44-56.
[2]VALIENTE M, MARIN O. Neuronal migration mechanisms in development and disease [J]. Current opinion in neurobiology,2010,20(1):68-78.
[3]LIU J S. Molecular genetics of neuronal migration disorders [J]. Current neurology and neuroscience reports,2011,11(2):171-8.
[4]MANZINI M C, WALSH C A. What disorders of cortical development tell us about the cortex:one plus one does not always make two [J]. Current opinion in genetics & development,2011,21(3):333-9.
[5]RUBENSTEIN J L. Annual Research Review:Development of the cerebral cortex:implications for neurodevelopmental disorders [J]. Journal of child psychology and psychiatry, and allied disciplines,2011,52(4):339-55.
[6]JONES E G. Neurotransmitters in the cerebral cortex [J]. Journal of neurosurgery,1986,65(2):135-53.
[7]DEFELIPE J, FARINAS I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs [J]. Progress in neurobiology,1992,39(6):563-607.
[8]O'LEARY D D, KOESTER S E. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex [J]. Neuron, 1993,10(6):991-1006.
[9]MOLYNEAUX B J, ARLOTTA P, MENEZES J R, et al. Neuronal subtype specification in the cerebral cortex [J]. Nature reviews Neuroscience,2007,8(6): 427-37.
[10]MARKRAM H, TOLEDO-RODRIGUEZ M, WANG Y, et al. Interneurons of the neocortical inhibitory system [J]. Nature reviews Neuroscience,2004,5(10): 793-807.
[11]MIYOSHI G, BUTT S J, TAKEBAYASHI H, et al. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-龙江 expressing precursors [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2007,27(29):7786-98.
[12]MIYOSHI G, FISHELL G. GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development [J]. Cerebral cortex, 2011,21(4):845-52.
[13]MARIN O, RUBENSTEIN J L. Cell migration in the forebrain [J]. Annual review of neuroscience,2003,26(441-83.
[14]RASH B G, GROVE E A. Area and layer patterning in the developing cerebral cortex [J]. Current opinion in neurobiology,2006,16(1):25-34.
[15]WONDERS C P, ANDERSON S A. The origin and specification of cortical interneurons [J]. Nature reviews Neuroscience,2006,7(9):687-96.
[16]LEONE D P, SRINIVASAN K, CHEN B, et al. The determination of projection neuron identity in the developing cerebral cortex [J]. Current opinion in neurobiology,2008,18(1):28-35.
[17]BATISTA-BRITO R, FISHELL G The developmental integration of cortical interneurons into a functional network [J]. Current topics in developmental biology,2009,87(81-118.
[18]MONUKI E S, WALSH C A. Mechanisms of cerebral cortical patterning in mice and humans [J]. Nature neuroscience,2001,4 Suppl(1199-206.
[19]HEVNER R F, SHI L, JUSTICE N, et al. Tbrl regulates differentiation of the preplate and layer 6 [J]. Neuron,2001,29(2):353-66.
[20]MALLAMACI A, STOYKOVA A. Gene networks controlling early cerebral cortex arealization [J]. Eur J Neurosci,2006,23(4):847-56.
[21]GUILLEMOT F. Cell fate specification in the mammalian telencephalon [J]. Progress in neurobiology,2007,83(1):37-52.
[22]HEBERT J M, FISHELL G. The genetics of early telencephalon patterning: some assembly required [J]. Nature reviews Neuroscience,2008,9(9):678-85.
[23]O'LEARY D D, SAHARA S. Genetic regulation of arealization of the neocortex [J]. Current opinion in neurobiology,2008,18(1):90-100.
[24]CHOLFIN J A, RUBENSTEIN J L. Patterning of frontal cortex subdivisions by Fgf17 [J]. Proceedings of the National Academy of Sciences of the United States of America,2007,104(18):7652-7.
[25]CHOLFIN J A, RUBENSTEIN J L. Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2 [J]. The Journal of comparative neurology,2008,509(2):144-55.
[26]HOCH R V, RUBENSTEIN J L, PLEASURE S. Genes and signaling events that establish regional patterning of the mammalian forebrain [J]. Seminars in cell & developmental biology,2009,20(4):378-86.
[27]SANSOM S N, LIVESEY F J. Gradients in the brain:the control of the development of form and function in the cerebral cortex [J]. Cold Spring Harbor perspectives in biology,2009,1(2):a002519.
[28]O'LEARY D D, CHOU S J, SAHARA S. Area patterning of the mammalian cortex [J]. Neuron,2007,56(2):252-69.
[29]RAKIC P, AYOUB A E, BREUNIG J J, et al. Decision by division:making cortical maps [J]. Trends in neurosciences,2009,32(5):291-301.
[30]PETANJEK Z, BERGER B, ESCLAPEZ M. Origins of cortical GABAergic neurons in the cynomolgus monkey [J]. Cerebral cortex,2009,19(2):249-62.
[31]MIYOSHI G, HJERLING-LEFFLER J, KARAYANNIS T, et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2010,30(5): 1582-94.
[32]LUI J H, HANSEN D V, KRIEGSTEIN A R. Development and evolution of the human neocortex [J]. Cell,2011,146(1):18-36.
[33]SAHARA S, O'LEARY D D. Fgf10 regulates transition period of cortical stem cell differentiation to radial glia controlling generation of neurons and basal progenitors [J]. Neuron,2009,63(1):48-62.
[34]MERKLE F T, ALVAREZ-BUYLLA A. Neural stem cells in mammalian development [J]. Current opinion in cell biology,2006,18(6):704-9.
[35]KANG W, WONG L C, SHI S H, et al. The transition from radial glial to intermediate progenitor cell is inhibited by FGF signaling during corticogenesis [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2009,29(46):14571-80.
[36][KRIEGSTEIN A, NOCTOR S, MARTINEZ-CERDENO V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion [J]. Nature reviews Neuroscience,2006,7(11):883-90.
[37]ELIAS L A, POTTER G B, KRIEGSTEIN A R. A time and a place for nkx2-1 in interneuron specification and migration [J]. Neuron,2008,59(5):679-82.
[38]MEROT Y, RETAUX S, HENG J I. Molecular mechanisms of projection neuron production and maturation in the developing cerebral cortex [J]. Seminars in cell & developmental biology,2009,20(6):726-34.
[39]SUBRAMANIAN L, TOLE S. Mechanisms underlying the specification, positional regulation, and function of the cortical hem [J]. Cerebral cortex,2009, 19 Suppl 1(190-5.
[40]THORNTON G K, WOODS C G. Primary microcephaly:do all roads lead to Rome? [J]. Trends in genetics:TIG,2009,25(11):501-10.
[41]YU T W, MOCHIDA G H, TISCHFIELD D J, et al. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture [J]. Nature genetics,2010,42(11): 1015-20.
[42]CASTIEL A, DANIELI M M, DAVID A, et al. The Stil protein regulates centrosome integrity and mitosis through suppression of Chfr [J]. Journal of cell science,2011,124(Pt4):532-9.
[43]KALAY E, YIGIT G, ASLAN Y, et al. CEP152 is a genome maintenance protein disrupted in Seckel syndrome [J]. Nature genetics,2011,43(1):23-6.
[44]WYNSHAW-BORIS A. Lissencephaly and LIS1:insights into the molecular mechanisms of neuronal migration and development [J]. Clinical genetics,2007, 72(4):296-304.
[45]FERLAND R J, BATIZ L F, NEAL J, et al. Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia [J]. Human molecular genetics,2009,18(3):497-516.
[46]PRAMPARO T, YOUN Y H, YINGLING J, et al. Novel embryonic neuronal migration and proliferation defects in Dcx mutant mice are exacerbated by Lisl reduction [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2010,30(8):3002-12.
[47]POIRIER K, KEAYS D A, FRANCIS F, et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A) [J]. Human mutation,2007,28(11):1055-64.
[48]ABDOLLAHI M R, MORRISON E, SIREY T, et al. Mutation of the variant alpha-tubulin TUBA8 results in polymicrogyria with optic nerve hypoplasia [J]. American journal of human genetics,2009,85(5):737-44.
[49]JAGLIN X H, CHELLY J. Tubulin-related cortical dysgeneses:microtubule dysfunction underlying neuronal migration defects [J]. Trends in genetics:TIG, 2009,25(12):555-66.
[50]KUMAR A, GIRIMAJI S C, DUVVARI M R, et al. Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly [J]. American journal of human genetics,2009,84(2):286-90.
[51]POIRIER K, SAILLOUR Y, BAHI-BUISSON N, et al. Mutations in the neuronal ss-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects [J]. Human molecular genetics, 2010,19(22):4462-73.
[52]HENG J I, NGUYEN L, CASTRO D S, et al. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2 [J]. Nature,2008,455(7209): 114-8.
[53]NOBREGA-PEREIRA S, KESSARIS N, DU T, et al. Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors [J]. Neuron,2008,59(5):733-45.
[54]HERNANDEZ-MIRANDA L R, CARIBONI A, FAUX C, et al. Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2011,31(16):6174-87.
[55]CHEN B, WANG S S, HATTOX A M, et al. The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex [J]. Proceedings of the National Academy of Sciences of the United States of America,2008,105(32):11382-7.
[56]LAI T, JABAUDON D, MOLYNEAUX B J, et al. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes [J]. Neuron,2008,57(2): 232-47.
[57]HEVNER R F. Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development [J]. Journal of neuropathology and experimental neurology,2007,66(2):101-9.
[58]GARBELLI R, ROSSINI L, MORONI R F, et al. Layer-specific genes reveal a rudimentary laminar pattern in human nodular heterotopia [J]. Neurology,2009, 73(10):746-53.
[59]SIEGENTHALER J A, ASHIQUE A M, ZARBALIS K, et al. Retinoic acid from the meninges regulates cortical neuron generation [J]. Cell,2009,139(3): 597-609.
[60]BORRELL V, MARIN O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling [J]. Nature neuroscience,2006,9(10):1284-93.
[61]RADAKOVITS R, BARROS C S, BELVINDRAH R, et al. Regulation of radial glial survival by signals from the meninges [J]. The Journal of neuroscience: the official journal of the Society for Neuroscience,2009,29(24):7694-705.
[62]INOUE T, OGAWA M, MIKOSHIBA K, et al. Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type Ⅱ lissencephaly [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(18):4712-25.
[63]HECHT J H, SIEGENTHALER J A, PATTERSON K P, et al. Primary cellular meningeal defects cause neocortical dysplasia and dyslamination [J]. Annals of neurology,2010,68(4):454-64.
[64]BARKOVICH A J. Subcortical heterotopia:a distinct clinicoradiologic entity [J]. AJNR American journal of neuroradiology,1996,17(7):1315-22.
[65]BARKOVICH A J. Morphologic characteristics of subcortical heterotopia:MR imaging study [J]. AJNR American journal of neuroradiology,2000,21(2): 290-5.
[66]BARKOVICH A J. Current concepts of polymicrogyria [J]. Neuroradiology, 2010,52(6):479-87.
[67]BARTH P G, ARONICA E, DE VRIES L, et al. Pontocerebellar hypoplasia type 2:a neuropathological update [J]. Acta neuropathologica,2007,114(4):373-86.
[68]NAMAVAR Y, BARTH P G, KASHER P R, et al. Clinical, neuroradiological and genetic findings in pontocerebellar hypoplasia [J]. Brain:a journal of neurology,2011,134(Pt 1):143-56.
[69]NAJM J, HORN D, WIMPLINGER I, et al. Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum [J]. Nature genetics,2008,40(9):1065-7.
[70]TAKANASHI J, ARAI H, NABATAME S, et al. Neuroradiologic features of CASK mutations [J]. AJNR American journal of neuroradiology,2010,31(9): 1619-22.
[71]KORTUM F, DAS S, FLINDT M, et al. The core FOXG1 syndrome phenotype consists of postnatal microcephaly, severe mental retardation, absent language, dyskinesia, and corpus callosum hypogenesis [J]. Journal of medical genetics, 2011,48(6):396-406.
[72]FERLAND R J, GAITANIS J N, APSE K, et al. Periventricular nodular heterotopia and Williams syndrome [J]. American journal of medical genetics Part A,2006,140(12):1305-11.
[73]CONWAY R L, PRESSMAN B D, DOBYNS W B, et al. Neuroimaging findings in macrocephaly-capillary malformation:a longitudinal study of 17 patients [J]. American journal of medical genetics Part A,2007,143A(24): 2981-3008.
[74]CRINO P B, NATHANSON K L, HENSKE E P. The tuberous sclerosis complex [J]. The New England journal of medicine,2006,355(13):1345-56.
[75]DE VRIES P J. Targeted treatments for cognitive and neurodevelopmental disorders in tuberous sclerosis complex [J]. Neurotherapeutics:the journal of the American Society for Experimental NeuroTherapeutics,2010,7(3):275-82.
[76]MORRIS-ROSENDAHL D J, NAJM J, LACHMEIJER A M, et al. Refining the phenotype of alpha-la Tubulin (TUBA1A) mutation in patients with classical lissencephaly [J]. Clinical genetics,2008,74(5):425-33.
[77]KUMAR R A, PILZ D T, BABATZ T D, et al. TUBA1A mutations cause wide spectrum lissencephaly (smooth brain) and suggest that multiple neuronal migration pathways converge on alpha tubulins [J]. Human molecular genetics, 2010,19(14):2817-27.
[78]BAHI-BUISSON N, POIRIER K, BODDAERT N, et al. GPR56-related bilateral frontoparietal polymicrogyria:further evidence for an overlap with the cobblestone complex [J]. Brain:a journal of neurology,2010,133(11): 3194-209.
[79]BARKOVICH A J, PEACOCK W. Sublobar dysplasia:a new malformation of cortical development [J]. Neurology,1998,50(5):1383-7.
[80]TUXHORN I, WOERMANN F G, PANNEK H W, et al. Sublobar dysplasia--A clinicopathologic report after successful epilepsy surgery [J]. Epilepsia,2009, 50(12):2652-7.
[81]HEWITT J E. Abnormal glycosylation of dystroglycan in human genetic disease [J]. Biochimica et biophysica acta,2009,1792(9):853-61.
[82]ACKROYD M R, WHITMORE C, PRIOR S, et al. Fukutin-related protein alters the deposition of laminin in the eye and brain [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2011,31(36): 12927-35.
[83]LUO R, JEONG S J, JIN Z, et al. G protein-coupled receptor 56 and collagen Ⅲ, a receptor-ligand pair, regulates cortical development and lamination [J]. Proceedings of the National Academy of Sciences of the United States of America,2011,108(31):12925-30.
[84]LI S, JIN Z, KOIRALA S, et al. GPR56 regulates pial basement membrane integrity and cortical lamination [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(22):5817-26.
[85]JUDKINS A R, MARTINEZ D, FERREIRA P, et al. Polymicrogyria includes fusion of the molecular layer and decreased neuronal populations but normal cortical laminar organization [J]. Journal of neuropathology and experimental neurology,2011,70(6):438-43.
[86]GRANATA T, FARINA L, FAIELLA A, et al. Familial schizencephaly associated with EMX2 mutation [J]. Neurology,1997,48(5):1403-6.
[87]TIETJEN I, BODELL A, APSE K, et al. Comprehensive EMX2 genotyping of a large schizencephaly case series [J]. American journal of medical genetics Part A,2007,143A(12):1313-6.
[88]MERELLO E, SWANSON E, DE MARCO P, et al. No major role for the EMX2 gene in schizencephaly [J]. American journal of medical genetics Part A, 2008,146A(9):1142-50.
[89]CURRY C J, LAMMER E J, NELSON V, et al. Schizencephaly:heterogeneous etiologies in a population of 4 million California births [J]. American journal of medical genetics Part A,2005,137(2):181-9.
[90]MARIN-PADILLA M, PARISI J E, ARMSTRONG D L, et al. Shaken infant syndrome:developmental neuropathology, progressive cortical dysplasia, and epilepsy [J]. Acta neuropathologica,2002,103(4):321-32.
[91]KRSEK P, JAHODOVA A, MATON B, et al. Low-grade focal cortical dysplasia is associated with prenatal and perinatal brain injury [J]. Epilepsia,2010,51(12): 2440-8.
[92]SAITO T, HANAI S, TAKASHIMA S, et al. Neocortical layer formation of human developing brains and lissencephalies:consideration of layer-specific marker expression [J]. Cerebral cortex,2011,21(3):588-96.
[93]NIETO M, MONUKI E S, TANG H, et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex [J]. The Journal of comparative neurology,2004,479(2):168-80.
[94]BRITANOVA O, DE JUAN ROMERO C, CHEUNG A, et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex [J]. Neuron,2008,57(3):378-92.
[95]SHEEN V L, FERLAND R J, NEAL J, et al. Neocortical neuronal arrangement in Miller Dieker syndrome [J]. Acta neuropathologica,2006,111(5):489-96.
[96]ARLOTTA P, MOLYNEAUX B J, CHEN J, et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo [J]. Neuron, 2005,45(2):207-21.
[97]FERLAND R J, CHERRY T J, PREWARE P O, et al. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain [J]. The Journal of comparative neurology,2003,460(2):266-79.
[98]HEVNER R F, MIYASHITA-LIN E, RUBENSTEIN J L. Cortical and thalamic axon pathfinding defects in Tbrl, Gbx2, and Pax6 mutant mice:evidence that cortical and thalamic axons interact and guide each other [J]. The Journal of comparative neurology,2002,447(1):8-17.
[99]GUILLEMOT F, MOLNAR Z, TARABYKIN V, et al. Molecular mechanisms of cortical differentiation [J]. Eur J Neurosci,2006,23(4):857-68.
[2]MORONI R F, CIPELLETTI B, INVERARDI F, et al. Development of cortical malformations in BCNU-treated rat, model of cortical dysplasia [J]. Neuros-cience,2011,175(380-93.
[3]BENARDETE E A, KRIEGSTEIN A R. Increased excitability and decreased sensitivity to GAB A in an animal model of dysplastic cortex [J]. Epilepsia,2002, 43(9):970-82.
[4]WIMMER V C, REID C A, SO E Y, et al. Axon initial segment dysfunction in epilepsy [J]. The Journal of physiology,2010,588(Pt 11):1829-40.
[5]SUN X Z, TAKAHASHI S, FUKUI Y, et al. Neurogenesis of heterotopic gray matter in the brain of the microcephalic mouse [J]. Journal of neuroscience research,2001,66(6):1083-93.
[6]BATTAGLIA G, PAGLIARDINI S, SAGLIETTI L, et al. Neurogenesis in cerebral heterotopia induced in rats by prenatal methylazoxymethanol treatment [J]. Cerebral cortex,2003,13(7):736-48.
[7]POLUCH S, JULIANO S L. A normal radial glial scaffold is necessary for migration of interneurons during neocortical development [J]. Glia,2007,55(8): 822-30.
[8]WONG M. Animal models of focal cortical dysplasia and tuberous sclerosis complex:recent progress toward clinical applications [J]. Epilepsia,2009,50 Suppl 9(34-44.
[9]MORONI R F, INVERARDI F, REGONDI M C, et al. Expression of layer-specific markers in the adult neocortex of BCNU-Treated rat, a model of cortical dysplasia [J]. Neuroscience,2009,159(2):682-91.
[10]ZIMMER C, TIVERON M C, BODMER R, et al. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons [J]. Cerebral cortex,2004,14(12):1408-20.
[11]YONESHIMA H, YAMASAKI S, VOELKER C C, et al. Er81 is expressed in a subpopulation of layer 5 neurons in rodent and primate neocortices [J]. Neuroscience,2006,137(2):401-12.
[12]WATAKABE A, ICHINOHE N, OHSAWA S, et al. Comparative analysis of layer-specific genes in Mammalian neocortex [J]. Cerebral cortex,2007,17(8): 1918-33.
[13]FERRER I, BERNET E, SORIANO E, et al. Naturally occurring cell death in the cerebral cortex of the rat and removal of dead cells by transitory phagocytes [J]. Neuroscience,1990,39(2):451-8.
[14]SPREAFICO R, FRASSONI C, ARCELLI P, et al. In situ labeling of apoptotic cell death in the cerebral cortex and thalamus of rats during development [J]. The Journal of comparative neurology,1995,363(2):281-95.
[15]DALMAU I, VELA J M, GONZALEZ B, et al. Dynamics of microglia in the developing rat brain [J]. The Journal of comparative neurology,2003,458(2): 144-57.
[16]MORONI R F, INVERARDI F, REGONDI M C, et al. Altered spatial distribution of PV-cortical cells and dysmorphic neurons in the somatosensory cortex of BCNU-treated rat model of cortical dysplasia [J]. Epilepsia,2008, 49(5):872-87.
[17]GARBELLI R, MUNARI C, DE BIASI S, et al. Taylor's cortical dysplasia:a confocal and ultrastructural immunohistochemical study [J]. Brain pathology, 1999,9(3):445-61.
[18]SPREAFICO R, TASSI L, COLOMBO N, et al. Inhibitory circuits in human dysplastic tissue [J]. Epilepsia,2000,41 Suppl 6(S 168-73.
[19]CRINO P B, DUHAIME A C, BALTUCH G, et al. Differential expression of glutamate and GAB A-A receptor subunit mRNA in cortical dysplasia [J]. Neurology,2001,56(7):906-13.
[20]OGHLAKIAN R O, TILELLI C Q, HIREMATH G K, et al. Single injection of a low dose of pentylenetetrazole leads to epileptogenesis in an animal model of cortical dysplasia [J]. Epilepsia,2009,50(4):801-10.
[21]KELLINGHAUS C, MODDEL G, SHIGETO H, et al. Dissociation between in vitro and in vivo epileptogenicity in a rat model of cortical dysplasia [J]. Epile-ptic disorders:international epilepsy journal with videotape,2007,9(1):11-9.
[22]LONG L L, XIAO B, SONG Y M, et al. [Changes of expression of cation-chloride cotransporter genes in hippocampus of cortical dysplasia: experiment with rat] [J]. Zhonghua yi xue za zhi,2007,87(19):1351-4.
[23]NIETO M, MONUKI E S, TANG H, et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex [J]. The Journal of comparative neurology,2004,479(2):168-80.
[24]BRITANOVA O, DE JUAN ROMERO C, CHEUNG A, et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex [J]. Neuron,2008,57(3):378-92.
[25]SHEEN V L, FERLAND R J, NEAL J, et al. Neocortical neuronal arrangement in Miller Dieker syndrome [J]. Acta neuropathologica,2006,111(5):489-96.
[26]ARLOTTA P, MOLYNEAUX B J, CHEN J, et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo [J]. Neuron, 2005,45(2):207-21.
[27]HEVNER R F, SHI L, JUSTICE N, et al. Tbrl regulates differentiation of the preplate and layer 6 [J]. Neuron,2001,29(2):353-66.
[28]FERLAND R J, CHERRY T J, PREWARE P O, et al. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain [J]. The Journal of comparative neurology,2003,460(2):266-79.
[29]HEVNER R F, MIYASHITA-LIN E, RUBENSTEIN J L. Cortical and thalamic axon pathfinding defects in Tbrl, Gbx2, and Pax6 mutant mice:evidence that cortical and thalamic axons interact and guide each other [J]. The Journal of comparative neurology,2002,447(1):8-17.
[30]GUILLEMOT F, MOLNAR Z, TARABYKIN V, et al. Molecular mechanisms of cortical differentiation [J]. Eur J Neurosci,2006,23(4):857-68.
[31]LEONE D P, SRINIVASAN K, CHEN B, et al. The determination of projection neuron identity in the developing cerebral cortex [J]. Current opinion in neurobiology,2008,18(1):28-35.
[32]MATSUMOTO H, JIANG J Y, MITANI D, et al. Distribution and gene expression of cytoskeletal proteins in two-cell rat embryos and developmental arrest [J]. The Journal of experimental zoology,2002,293(7):641-8.
[33]LI S, JIN Z, KOIRALA S, et al. GPR56 regulates pial basement membrane integrity and cortical lamination [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(22):5817-26.
[34]OGAWA Y, RASBAND M N. The functional organization and assembly of the axon initial segment [J]. Current opinion in neurobiology,2008,18(3):307-13.
[35]RASBAND M N. The axon initial segment and the maintenance of neuronal polarity [J]. Nature reviews Neuroscience,2010,11(8):552-62.
[36]KOLE M H, ILSCHNER S U, KAMPA B M, et al. Action potential generation requires a high sodium channel density in the axon initial segment [J]. Nature neuroscience,2008,11(2):178-86.
[37]KOLE M H, LETZKUS J J, STUART G J. Axon initial segment Kvl channels control axonal action potential waveform and synaptic efficacy [J]. Neuron, 2007,55(4):633-47.
[38]GOLDBERG E M, CLARK B D, ZAGHA E, et al. K+ channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons [J]. Neuron,2008,58(3):387-400.
[39]NAUNDORF B, WOLF F, VOLGUSHEV M. Unique features of action potential initiation in cortical neurons [J]. Nature,2006,440(7087):1060-3.
[40]SCHAFER D P, JHA S, LIU F, et al. Disruption of the axon initial segment cytoskeleton is a new mechanism for neuronal injury [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2009,29(42): 13242-54.
[41]KUBA H, OICHI Y, OHMORI H. Presynaptic activity regulates Na(+) channel distribution at the axon initial segment [J]. Nature,2010,465(7301):1075-8.
[42]GRUBB M S, BURRONE J. Activity-dependent relocation of the axon initial segment fine-tunes neuronal excitability [J]. Nature,2010,465(7301):1070-4.
[43]GRUNDEMANN J, HAUSSER M. Neuroscience:A plastic axonal hotspot [J]. Nature,2010,465(7301):1022-3.
[44]HINMAN J D, RASBAND M N, CARMICHAEL S T. Remodeling of the axon initial segment after focal cortical and white matter stroke [J]. Stroke; a journal of cerebral circulation,2013,44(1):182-9.
[45]WIMMER V C, REID C A, MITCHELL S, et al. Axon initial segment dysfunction in a mouse model of genetic epilepsy with febrile seizures plus [J]. The Journal of clinical investigation,2010,120(8):2661-71.
[46]THOMAS E A, HAWKINS R J, RICHARDS K L, et al. Heat opens axon initial segment sodium channels:a febrile seizure mechanism? [J]. Annals of neurology,2009,66(2):219-26.
[47]BLUMENFELD H, LAMPERT A, KLEIN J P, et al. Role of hippocampal sodium channel Navl.6 in kindling epileptogenesis [J]. Epilepsia,2009,50(1): 44-55.
[48]HUANG Z J, DI CRISTO G, ANGO F. Development of GABA innervation in the cerebral and cerebellar cortices [J]. Nature reviews Neuroscience,2007,8(9): 673-86.
[49]FAIREN A, VALVERDE F. A specialized type of neuron in the visual cortex of cat:a Golgi and electron microscope study of chandelier cells [J]. The Journal of comparative neurology,1980,194(4):761-79.
[50]DEFELIPE J. Chandelier cells and epilepsy [J]. Brain:a journal of neurology, 1999,122 (Pt10)(1807-22.
[1]KUZNIECKY R I. Magnetic resonance imaging in developmental disorders of the cerebral cortex [J]. Epilepsia,1994,35 Suppl 6(S44-56.
[2]VALIENTE M, MARIN O. Neuronal migration mechanisms in development and disease [J]. Current opinion in neurobiology,2010,20(1):68-78.
[3]LIU J S. Molecular genetics of neuronal migration disorders [J]. Current neurology and neuroscience reports,2011,11(2):171-8.
[4]MANZINI M C, WALSH C A. What disorders of cortical development tell us about the cortex:one plus one does not always make two [J]. Current opinion in genetics & development,2011,21(3):333-9.
[5]RUBENSTEIN J L. Annual Research Review:Development of the cerebral cortex:implications for neurodevelopmental disorders [J]. Journal of child psychology and psychiatry, and allied disciplines,2011,52(4):339-55.
[6]JONES E G. Neurotransmitters in the cerebral cortex [J]. Journal of neurosurgery,1986,65(2):135-53.
[7]DEFELIPE J, FARINAS I. The pyramidal neuron of the cerebral cortex: morphological and chemical characteristics of the synaptic inputs [J]. Progress in neurobiology,1992,39(6):563-607.
[8]O'LEARY D D, KOESTER S E. Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex [J]. Neuron, 1993,10(6):991-1006.
[9]MOLYNEAUX B J, ARLOTTA P, MENEZES J R, et al. Neuronal subtype specification in the cerebral cortex [J]. Nature reviews Neuroscience,2007,8(6): 427-37.
[10]MARKRAM H, TOLEDO-RODRIGUEZ M, WANG Y, et al. Interneurons of the neocortical inhibitory system [J]. Nature reviews Neuroscience,2004,5(10): 793-807.
[11]MIYOSHI G, BUTT S J, TAKEBAYASHI H, et al. Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-龙江 expressing precursors [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2007,27(29):7786-98.
[12]MIYOSHI G, FISHELL G. GABAergic interneuron lineages selectively sort into specific cortical layers during early postnatal development [J]. Cerebral cortex, 2011,21(4):845-52.
[13]MARIN O, RUBENSTEIN J L. Cell migration in the forebrain [J]. Annual review of neuroscience,2003,26(441-83.
[14]RASH B G, GROVE E A. Area and layer patterning in the developing cerebral cortex [J]. Current opinion in neurobiology,2006,16(1):25-34.
[15]WONDERS C P, ANDERSON S A. The origin and specification of cortical interneurons [J]. Nature reviews Neuroscience,2006,7(9):687-96.
[16]LEONE D P, SRINIVASAN K, CHEN B, et al. The determination of projection neuron identity in the developing cerebral cortex [J]. Current opinion in neurobiology,2008,18(1):28-35.
[17]BATISTA-BRITO R, FISHELL G The developmental integration of cortical interneurons into a functional network [J]. Current topics in developmental biology,2009,87(81-118.
[18]MONUKI E S, WALSH C A. Mechanisms of cerebral cortical patterning in mice and humans [J]. Nature neuroscience,2001,4 Suppl(1199-206.
[19]HEVNER R F, SHI L, JUSTICE N, et al. Tbrl regulates differentiation of the preplate and layer 6 [J]. Neuron,2001,29(2):353-66.
[20]MALLAMACI A, STOYKOVA A. Gene networks controlling early cerebral cortex arealization [J]. Eur J Neurosci,2006,23(4):847-56.
[21]GUILLEMOT F. Cell fate specification in the mammalian telencephalon [J]. Progress in neurobiology,2007,83(1):37-52.
[22]HEBERT J M, FISHELL G. The genetics of early telencephalon patterning: some assembly required [J]. Nature reviews Neuroscience,2008,9(9):678-85.
[23]O'LEARY D D, SAHARA S. Genetic regulation of arealization of the neocortex [J]. Current opinion in neurobiology,2008,18(1):90-100.
[24]CHOLFIN J A, RUBENSTEIN J L. Patterning of frontal cortex subdivisions by Fgf17 [J]. Proceedings of the National Academy of Sciences of the United States of America,2007,104(18):7652-7.
[25]CHOLFIN J A, RUBENSTEIN J L. Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2 [J]. The Journal of comparative neurology,2008,509(2):144-55.
[26]HOCH R V, RUBENSTEIN J L, PLEASURE S. Genes and signaling events that establish regional patterning of the mammalian forebrain [J]. Seminars in cell & developmental biology,2009,20(4):378-86.
[27]SANSOM S N, LIVESEY F J. Gradients in the brain:the control of the development of form and function in the cerebral cortex [J]. Cold Spring Harbor perspectives in biology,2009,1(2):a002519.
[28]O'LEARY D D, CHOU S J, SAHARA S. Area patterning of the mammalian cortex [J]. Neuron,2007,56(2):252-69.
[29]RAKIC P, AYOUB A E, BREUNIG J J, et al. Decision by division:making cortical maps [J]. Trends in neurosciences,2009,32(5):291-301.
[30]PETANJEK Z, BERGER B, ESCLAPEZ M. Origins of cortical GABAergic neurons in the cynomolgus monkey [J]. Cerebral cortex,2009,19(2):249-62.
[31]MIYOSHI G, HJERLING-LEFFLER J, KARAYANNIS T, et al. Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2010,30(5): 1582-94.
[32]LUI J H, HANSEN D V, KRIEGSTEIN A R. Development and evolution of the human neocortex [J]. Cell,2011,146(1):18-36.
[33]SAHARA S, O'LEARY D D. Fgf10 regulates transition period of cortical stem cell differentiation to radial glia controlling generation of neurons and basal progenitors [J]. Neuron,2009,63(1):48-62.
[34]MERKLE F T, ALVAREZ-BUYLLA A. Neural stem cells in mammalian development [J]. Current opinion in cell biology,2006,18(6):704-9.
[35]KANG W, WONG L C, SHI S H, et al. The transition from radial glial to intermediate progenitor cell is inhibited by FGF signaling during corticogenesis [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2009,29(46):14571-80.
[36][KRIEGSTEIN A, NOCTOR S, MARTINEZ-CERDENO V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion [J]. Nature reviews Neuroscience,2006,7(11):883-90.
[37]ELIAS L A, POTTER G B, KRIEGSTEIN A R. A time and a place for nkx2-1 in interneuron specification and migration [J]. Neuron,2008,59(5):679-82.
[38]MEROT Y, RETAUX S, HENG J I. Molecular mechanisms of projection neuron production and maturation in the developing cerebral cortex [J]. Seminars in cell & developmental biology,2009,20(6):726-34.
[39]SUBRAMANIAN L, TOLE S. Mechanisms underlying the specification, positional regulation, and function of the cortical hem [J]. Cerebral cortex,2009, 19 Suppl 1(190-5.
[40]THORNTON G K, WOODS C G. Primary microcephaly:do all roads lead to Rome? [J]. Trends in genetics:TIG,2009,25(11):501-10.
[41]YU T W, MOCHIDA G H, TISCHFIELD D J, et al. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture [J]. Nature genetics,2010,42(11): 1015-20.
[42]CASTIEL A, DANIELI M M, DAVID A, et al. The Stil protein regulates centrosome integrity and mitosis through suppression of Chfr [J]. Journal of cell science,2011,124(Pt4):532-9.
[43]KALAY E, YIGIT G, ASLAN Y, et al. CEP152 is a genome maintenance protein disrupted in Seckel syndrome [J]. Nature genetics,2011,43(1):23-6.
[44]WYNSHAW-BORIS A. Lissencephaly and LIS1:insights into the molecular mechanisms of neuronal migration and development [J]. Clinical genetics,2007, 72(4):296-304.
[45]FERLAND R J, BATIZ L F, NEAL J, et al. Disruption of neural progenitors along the ventricular and subventricular zones in periventricular heterotopia [J]. Human molecular genetics,2009,18(3):497-516.
[46]PRAMPARO T, YOUN Y H, YINGLING J, et al. Novel embryonic neuronal migration and proliferation defects in Dcx mutant mice are exacerbated by Lisl reduction [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2010,30(8):3002-12.
[47]POIRIER K, KEAYS D A, FRANCIS F, et al. Large spectrum of lissencephaly and pachygyria phenotypes resulting from de novo missense mutations in tubulin alpha 1A (TUBA1A) [J]. Human mutation,2007,28(11):1055-64.
[48]ABDOLLAHI M R, MORRISON E, SIREY T, et al. Mutation of the variant alpha-tubulin TUBA8 results in polymicrogyria with optic nerve hypoplasia [J]. American journal of human genetics,2009,85(5):737-44.
[49]JAGLIN X H, CHELLY J. Tubulin-related cortical dysgeneses:microtubule dysfunction underlying neuronal migration defects [J]. Trends in genetics:TIG, 2009,25(12):555-66.
[50]KUMAR A, GIRIMAJI S C, DUVVARI M R, et al. Mutations in STIL, encoding a pericentriolar and centrosomal protein, cause primary microcephaly [J]. American journal of human genetics,2009,84(2):286-90.
[51]POIRIER K, SAILLOUR Y, BAHI-BUISSON N, et al. Mutations in the neuronal ss-tubulin subunit TUBB3 result in malformation of cortical development and neuronal migration defects [J]. Human molecular genetics, 2010,19(22):4462-73.
[52]HENG J I, NGUYEN L, CASTRO D S, et al. Neurogenin 2 controls cortical neuron migration through regulation of Rnd2 [J]. Nature,2008,455(7209): 114-8.
[53]NOBREGA-PEREIRA S, KESSARIS N, DU T, et al. Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors [J]. Neuron,2008,59(5):733-45.
[54]HERNANDEZ-MIRANDA L R, CARIBONI A, FAUX C, et al. Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2011,31(16):6174-87.
[55]CHEN B, WANG S S, HATTOX A M, et al. The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex [J]. Proceedings of the National Academy of Sciences of the United States of America,2008,105(32):11382-7.
[56]LAI T, JABAUDON D, MOLYNEAUX B J, et al. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes [J]. Neuron,2008,57(2): 232-47.
[57]HEVNER R F. Layer-specific markers as probes for neuron type identity in human neocortex and malformations of cortical development [J]. Journal of neuropathology and experimental neurology,2007,66(2):101-9.
[58]GARBELLI R, ROSSINI L, MORONI R F, et al. Layer-specific genes reveal a rudimentary laminar pattern in human nodular heterotopia [J]. Neurology,2009, 73(10):746-53.
[59]SIEGENTHALER J A, ASHIQUE A M, ZARBALIS K, et al. Retinoic acid from the meninges regulates cortical neuron generation [J]. Cell,2009,139(3): 597-609.
[60]BORRELL V, MARIN O. Meninges control tangential migration of hem-derived Cajal-Retzius cells via CXCL12/CXCR4 signaling [J]. Nature neuroscience,2006,9(10):1284-93.
[61]RADAKOVITS R, BARROS C S, BELVINDRAH R, et al. Regulation of radial glial survival by signals from the meninges [J]. The Journal of neuroscience: the official journal of the Society for Neuroscience,2009,29(24):7694-705.
[62]INOUE T, OGAWA M, MIKOSHIBA K, et al. Zic deficiency in the cortical marginal zone and meninges results in cortical lamination defects resembling those in type Ⅱ lissencephaly [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(18):4712-25.
[63]HECHT J H, SIEGENTHALER J A, PATTERSON K P, et al. Primary cellular meningeal defects cause neocortical dysplasia and dyslamination [J]. Annals of neurology,2010,68(4):454-64.
[64]BARKOVICH A J. Subcortical heterotopia:a distinct clinicoradiologic entity [J]. AJNR American journal of neuroradiology,1996,17(7):1315-22.
[65]BARKOVICH A J. Morphologic characteristics of subcortical heterotopia:MR imaging study [J]. AJNR American journal of neuroradiology,2000,21(2): 290-5.
[66]BARKOVICH A J. Current concepts of polymicrogyria [J]. Neuroradiology, 2010,52(6):479-87.
[67]BARTH P G, ARONICA E, DE VRIES L, et al. Pontocerebellar hypoplasia type 2:a neuropathological update [J]. Acta neuropathologica,2007,114(4):373-86.
[68]NAMAVAR Y, BARTH P G, KASHER P R, et al. Clinical, neuroradiological and genetic findings in pontocerebellar hypoplasia [J]. Brain:a journal of neurology,2011,134(Pt 1):143-56.
[69]NAJM J, HORN D, WIMPLINGER I, et al. Mutations of CASK cause an X-linked brain malformation phenotype with microcephaly and hypoplasia of the brainstem and cerebellum [J]. Nature genetics,2008,40(9):1065-7.
[70]TAKANASHI J, ARAI H, NABATAME S, et al. Neuroradiologic features of CASK mutations [J]. AJNR American journal of neuroradiology,2010,31(9): 1619-22.
[71]KORTUM F, DAS S, FLINDT M, et al. The core FOXG1 syndrome phenotype consists of postnatal microcephaly, severe mental retardation, absent language, dyskinesia, and corpus callosum hypogenesis [J]. Journal of medical genetics, 2011,48(6):396-406.
[72]FERLAND R J, GAITANIS J N, APSE K, et al. Periventricular nodular heterotopia and Williams syndrome [J]. American journal of medical genetics Part A,2006,140(12):1305-11.
[73]CONWAY R L, PRESSMAN B D, DOBYNS W B, et al. Neuroimaging findings in macrocephaly-capillary malformation:a longitudinal study of 17 patients [J]. American journal of medical genetics Part A,2007,143A(24): 2981-3008.
[74]CRINO P B, NATHANSON K L, HENSKE E P. The tuberous sclerosis complex [J]. The New England journal of medicine,2006,355(13):1345-56.
[75]DE VRIES P J. Targeted treatments for cognitive and neurodevelopmental disorders in tuberous sclerosis complex [J]. Neurotherapeutics:the journal of the American Society for Experimental NeuroTherapeutics,2010,7(3):275-82.
[76]MORRIS-ROSENDAHL D J, NAJM J, LACHMEIJER A M, et al. Refining the phenotype of alpha-la Tubulin (TUBA1A) mutation in patients with classical lissencephaly [J]. Clinical genetics,2008,74(5):425-33.
[77]KUMAR R A, PILZ D T, BABATZ T D, et al. TUBA1A mutations cause wide spectrum lissencephaly (smooth brain) and suggest that multiple neuronal migration pathways converge on alpha tubulins [J]. Human molecular genetics, 2010,19(14):2817-27.
[78]BAHI-BUISSON N, POIRIER K, BODDAERT N, et al. GPR56-related bilateral frontoparietal polymicrogyria:further evidence for an overlap with the cobblestone complex [J]. Brain:a journal of neurology,2010,133(11): 3194-209.
[79]BARKOVICH A J, PEACOCK W. Sublobar dysplasia:a new malformation of cortical development [J]. Neurology,1998,50(5):1383-7.
[80]TUXHORN I, WOERMANN F G, PANNEK H W, et al. Sublobar dysplasia--A clinicopathologic report after successful epilepsy surgery [J]. Epilepsia,2009, 50(12):2652-7.
[81]HEWITT J E. Abnormal glycosylation of dystroglycan in human genetic disease [J]. Biochimica et biophysica acta,2009,1792(9):853-61.
[82]ACKROYD M R, WHITMORE C, PRIOR S, et al. Fukutin-related protein alters the deposition of laminin in the eye and brain [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2011,31(36): 12927-35.
[83]LUO R, JEONG S J, JIN Z, et al. G protein-coupled receptor 56 and collagen Ⅲ, a receptor-ligand pair, regulates cortical development and lamination [J]. Proceedings of the National Academy of Sciences of the United States of America,2011,108(31):12925-30.
[84]LI S, JIN Z, KOIRALA S, et al. GPR56 regulates pial basement membrane integrity and cortical lamination [J]. The Journal of neuroscience:the official journal of the Society for Neuroscience,2008,28(22):5817-26.
[85]JUDKINS A R, MARTINEZ D, FERREIRA P, et al. Polymicrogyria includes fusion of the molecular layer and decreased neuronal populations but normal cortical laminar organization [J]. Journal of neuropathology and experimental neurology,2011,70(6):438-43.
[86]GRANATA T, FARINA L, FAIELLA A, et al. Familial schizencephaly associated with EMX2 mutation [J]. Neurology,1997,48(5):1403-6.
[87]TIETJEN I, BODELL A, APSE K, et al. Comprehensive EMX2 genotyping of a large schizencephaly case series [J]. American journal of medical genetics Part A,2007,143A(12):1313-6.
[88]MERELLO E, SWANSON E, DE MARCO P, et al. No major role for the EMX2 gene in schizencephaly [J]. American journal of medical genetics Part A, 2008,146A(9):1142-50.
[89]CURRY C J, LAMMER E J, NELSON V, et al. Schizencephaly:heterogeneous etiologies in a population of 4 million California births [J]. American journal of medical genetics Part A,2005,137(2):181-9.
[90]MARIN-PADILLA M, PARISI J E, ARMSTRONG D L, et al. Shaken infant syndrome:developmental neuropathology, progressive cortical dysplasia, and epilepsy [J]. Acta neuropathologica,2002,103(4):321-32.
[91]KRSEK P, JAHODOVA A, MATON B, et al. Low-grade focal cortical dysplasia is associated with prenatal and perinatal brain injury [J]. Epilepsia,2010,51(12): 2440-8.
[92]SAITO T, HANAI S, TAKASHIMA S, et al. Neocortical layer formation of human developing brains and lissencephalies:consideration of layer-specific marker expression [J]. Cerebral cortex,2011,21(3):588-96.
[93]NIETO M, MONUKI E S, TANG H, et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II-IV of the cerebral cortex [J]. The Journal of comparative neurology,2004,479(2):168-80.
[94]BRITANOVA O, DE JUAN ROMERO C, CHEUNG A, et al. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex [J]. Neuron,2008,57(3):378-92.
[95]SHEEN V L, FERLAND R J, NEAL J, et al. Neocortical neuronal arrangement in Miller Dieker syndrome [J]. Acta neuropathologica,2006,111(5):489-96.
[96]ARLOTTA P, MOLYNEAUX B J, CHEN J, et al. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo [J]. Neuron, 2005,45(2):207-21.
[97]FERLAND R J, CHERRY T J, PREWARE P O, et al. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain [J]. The Journal of comparative neurology,2003,460(2):266-79.
[98]HEVNER R F, MIYASHITA-LIN E, RUBENSTEIN J L. Cortical and thalamic axon pathfinding defects in Tbrl, Gbx2, and Pax6 mutant mice:evidence that cortical and thalamic axons interact and guide each other [J]. The Journal of comparative neurology,2002,447(1):8-17.
[99]GUILLEMOT F, MOLNAR Z, TARABYKIN V, et al. Molecular mechanisms of cortical differentiation [J]. Eur J Neurosci,2006,23(4):857-68.