Development and specification of GABAergic cortical interneurons

Cell & Bioscience

Wange Lu¹  Corey Kelsom¹ 

[1] Eli and Edythe Broad Center for Regenerative Medicine and Stem Cell Research, Department of Biochemistry and Molecular Biology, University of Southern California, 1425 San Pablo Street, Los Angeles, CA 90033, USA

关键词: Transcriptional network;    Specification;    Cortex;    Interneuron;    GABA;   

Others  :  798990
DOI  :  10.1186/2045-3701-3-19

 received in 2013-02-25, accepted in 2013-03-28,  发布年份 2013

【 摘 要 】

GABAergic interneurons are inhibitory neurons of the nervous system that play a vital role in neural circuitry and activity. They are so named due to their release of the neurotransmitter gamma-aminobutyric acid (GABA), and occupy different areas of the brain. This review will focus primarily on GABAergic interneurons of the mammalian cerebral cortex from a developmental standpoint. There is a diverse amount of cortical interneuronal subtypes that may be categorized by a number of characteristics; this review will classify them largely by the protein markers they express. The developmental origins of GABAergic interneurons will be discussed, as well as factors that influence the complex migration routes that these interneurons must take in order to ultimately localize in the cerebral cortex where they will integrate with the neural circuitry set in place. This review will also place an emphasis on the transcriptional network of genes that play a role in the specification and maintenance of GABAergic interneuron fate. Gaining an understanding of the different aspects of cortical interneuron development and specification, especially in humans, has many useful clinical applications that may serve to treat various neurological disorders linked to alterations in interneuron populations.

【 授权许可】

   
2013 Kelsom and Lu; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

【 参考文献 】

• [1]Hensch TK: Critical period plasticity in local cortical circuits. Nat Rev Neurosci 2005, 6(11):877-888.
• [2]Owens DF, Kriegstein AR: Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 2002, 3(9):715-727.
• [3]Wang XJ, Tegner J, Constantinidis C, Goldman-Rakic PS: Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc Natl Acad Sci U S A 2004, 101(5):1368-1373.
• [4]Whittington MA, Traub RD: Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci 2003, 26(12):676-682.
• [5]Dreifuss JJ, Kelly JS, Krnjevic K: Cortical inhibition and gamma-aminobutyric acid. Exp Brain Res 1969, 9(2):137-154.
• [6]Fonnum F, Storm-Mathisen J: GABA synthesis in rat hippocampus correlated to the distribution of inhibitory neurons. Acta Physiol Scand 1969, 76(1):35A-36A.
• [7]Somogyi P, Freund TF, Wu JY, Smith AD: The section-Golgi impregnation procedure. 2. Immunocytochemical demonstration of glutamate decarboxylase in Golgi-impregnated neurons and in their afferent synaptic boutons in the visual cortex of the cat. Neuroscience 1983, 9(3):475-490.
• [8]Rudy B, Fishell G, Lee S, Hjerling-Leffler J: Three groups of interneurons account for nearly 100% of neocortical GABAergic neurons. Dev Neurobiol 2011, 71(1):45-61.
• [9]Marin O: Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 2012, 13(2):107-120.
• [10]Gibson JR, Beierlein M, Connors BW: Two networks of electrically coupled inhibitory neurons in neocortex. Nature 1999, 402(6757):75-79.
• [11]Porter JT, Johnson CK, Agmon A: Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 2001, 21(8):2699-2710.
• [12]Berger TK, Silberberg G, Perin R, Markram H: Brief bursts self-inhibit and correlate the pyramidal network. PLoS Biol 2010, 8(9):e1000473.
• [13]Silberberg G, Gupta A, Markram H: Stereotypy in neocortical microcircuits. Trends Neurosci 2002, 25(5):227-230.
• [14]Wang Y, Toledo-Rodriguez M, Gupta A, Wu C, Silberberg G, Luo J, Markram H: Anatomical, physiological and molecular properties of Martinotti cells in the somatosensory cortex of the juvenile rat. J Physiol 2004, 561(Pt 1):65-90.
• [15]Somogyi P, Tamas G, Lujan R, Buhl EH: Salient features of synaptic organisation in the cerebral cortex. Brain Res Brain Res Rev 1998, 26(2–3):113-135.
• [16]Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A: Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 2008, 9(7):557-568.
• [17]Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J: Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 1997, 17(10):3894-3906.
• [18]DeFelipe J: Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex 1993, 3(4):273-289.
• [19]DeFelipe J, Hendry SH, Jones EG: Visualization of chandelier cell axons by parvalbumin immunoreactivity in monkey cerebral cortex. Proc Natl Acad Sci U S A 1989, 86(6):2093-2097.
• [20]Gonchar Y, Burkhalter A: Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 1997, 7(4):347-358.
• [21]Hendry SH, Jones EG, Emson PC, Lawson DE, Heizmann CW, Streit P: Two classes of cortical GABA neurons defined by differential calcium binding protein immunoreactivities. Exp Brain Res 1989, 76(2):467-472.
• [22]Kawaguchi Y, Kubota Y: GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 1997, 7(6):476-486.
• [23]Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C: Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 2004, 5(10):793-807.
• [24]Somogyi P, Klausberger T: Defined types of cortical interneurone structure space and spike timing in the hippocampus. J Physiol 2005, 562(Pt 1):9-26.
• [25]Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B: The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 2010, 30(50):16796-16808.
• [26]Xu X, Callaway EM: Laminar specificity of functional input to distinct types of inhibitory cortical neurons. J Neurosci 2009, 29(1):70-85.
• [27]Connors BW, Gutnick MJ: Intrinsic firing patterns of diverse neocortical neurons. Trends Neurosci 1990, 13(3):99-104.
• [28]Goldberg EM, Clark BD, Zagha E, Nahmani M, Erisir A, Rudy B: K + channels at the axon initial segment dampen near-threshold excitability of neocortical fast-spiking GABAergic interneurons. Neuron 2008, 58(3):387-400.
• [29]Pinto DJ, Brumberg JC, Simons DJ: Circuit dynamics and coding strategies in rodent somatosensory cortex. J Neurophysiol 2000, 83(3):1158-1166.
• [30]Miller LM, Escabi MA, Schreiner CE: Feature selectivity and interneuronal cooperation in the thalamocortical system. J Neurosci 2001, 21(20):8136-8144.
• [31]Pouille F, Scanziani M: Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 2001, 293(5532):1159-1163.
• [32]Pinto DJ, Hartings JA, Brumberg JC, Simons DJ: Cortical damping: analysis of thalamocortical response transformations in rodent barrel cortex. Cereb Cortex 2003, 13(1):33-44.
• [33]Lawrence JJ, McBain CJ: Interneuron diversity series: containing the detonation–feedforward inhibition in the CA3 hippocampus. Trends Neurosci 2003, 26(11):631-640.
• [34]Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M: Somatosensory integration controlled by dynamic thalamocortical feed-forward inhibition. Neuron 2005, 48(2):315-327.
• [35]Cruikshank SJ, Lewis TJ, Connors BW: Synaptic basis for intense thalamocortical activation of feedforward inhibitory cells in neocortex. Nat Neurosci 2007, 10(4):462-468.
• [36]Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA: Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 2005, 47(3):423-435.
• [37]Haider B, McCormick DA: Rapid neocortical dynamics: cellular and network mechanisms. Neuron 2009, 62(2):171-189.
• [38]Woodruff A, Xu Q, Anderson SA, Yuste R: Depolarizing effect of neocortical chandelier neurons. Frontiers in neural circuits 2009, 3:15.
• [39]Szabadics J, Varga C, Molnar G, Olah S, Barzo P, Tamas G: Excitatory effect of GABAergic axo-axonic cells in cortical microcircuits. Science 2006, 311(5758):233-235.
• [40]Glickfeld LL, Roberts JD, Somogyi P, Scanziani M: Interneurons hyperpolarize pyramidal cells along their entire somatodendritic axis. Nat Neurosci 2009, 12(1):21-23.
• [41]Blatow M, Rozov A, Katona I, Hormuzdi SG, Meyer AH, Whittington MA, Caputi A, Monyer H: A novel network of multipolar bursting interneurons generates theta frequency oscillations in neocortex. Neuron 2003, 38(5):805-817.
• [42]Uematsu M, Hirai Y, Karube F, Ebihara S, Kato M, Abe K, Obata K, Yoshida S, Hirabayashi M, Yanagawa Y: Quantitative chemical composition of cortical GABAergic neurons revealed in transgenic venus-expressing rats. Cereb Cortex 2008, 18(2):315-330.
• [43]Beierlein M, Gibson JR, Connors BW: Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 2003, 90(5):2987-3000.
• [44]Kapfer C, Glickfeld LL, Atallah BV, Scanziani M: Supralinear increase of recurrent inhibition during sparse activity in the somatosensory cortex. Nat Neurosci 2007, 10(6):743-753.
• [45]Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakmann B: Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 1998, 1(4):279-285.
• [46]Silberberg G, Markram H: Disynaptic inhibition between neocortical pyramidal cells mediated by Martinotti cells. Neuron 2007, 53(5):735-746.
• [47]Fanselow EE, Richardson KA, Connors BW: Selective, state-dependent activation of somatostatin-expressing inhibitory interneurons in mouse neocortex. J Neurophysiol 2008, 100(5):2640-2652.
• [48]Ma Y, Hu H, Berrebi AS, Mathers PH, Agmon A: Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J Neurosci 2006, 26(19):5069-5082.
• [49]McGarry LM, Packer AM, Fino E, Nikolenko V, Sippy T, Yuste R: Quantitative classification of somatostatin-positive neocortical interneurons identifies three interneuron subtypes. Front Neural Circ 2010, 4:12.
• [50]Xu X, Roby KD, Callaway EM: Mouse cortical inhibitory neuron type that coexpresses somatostatin and calretinin. J Comp Neurol 2006, 499(1):144-160.
• [51]Zimmer G, Rudolph J, Landmann J, Gerstmann K, Steinecke A, Gampe C, Bolz J: Bidirectional ephrinB3/EphA4 signaling mediates the segregation of medial ganglionic eminence- and preoptic area-derived interneurons in the deep and superficial migratory stream. J Neurosci 2011, 31(50):18364-18380.
• [52]Gonchar Y, Wang Q, Burkhalter A: Multiple distinct subtypes of GABAergic neurons in mouse visual cortex identified by triple immunostaining. Front Neuroanat 2007, 1:3.
• [53]Miyoshi G, Butt SJ, Takebayashi H, Fishell G: Physiologically distinct temporal cohorts of cortical interneurons arise from telencephalic Olig2-expressing precursors. J Neurosci 2007, 27(29):7786-7798.
• [54]Xu X, Roby KD, Callaway EM: Immunochemical characterization of inhibitory mouse cortical neurons: three chemically distinct classes of inhibitory cells. J Comp Neurol 2010, 518(3):389-404.
• [55]Cauli B, Porter JT, Tsuzuki K, Lambolez B, Rossier J, Quenet B, Audinat E: Classification of fusiform neocortical interneurons based on unsupervised clustering. Proc Natl Acad Sci U S A 2000, 97(11):6144-6149.
• [56]Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G: Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 2010, 30(5):1582-1594.
• [57]David C, Schleicher A, Zuschratter W, Staiger JF: The innervation of parvalbumin-containing interneurons by VIP-immunopositive interneurons in the primary somatosensory cortex of the adult rat. Eur J Neurosci 2007, 25(8):2329-2340.
• [58]Acsady L, Gorcs TJ, Freund TF: Different populations of vasoactive intestinal polypeptide-immunoreactive interneurons are specialized to control pyramidal cells or interneurons in the hippocampus. Neuroscience 1996, 73(2):317-334.
• [59]Ferezou I, Cauli B, Hill EL, Rossier J, Hamel E, Lambolez B: 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 2002, 22(17):7389-7397.
• [60]Galarreta M, Erdelyi F, Szabo G, Hestrin S: Electrical coupling among irregular-spiking GABAergic interneurons expressing cannabinoid receptors. J Neurosci 2004, 24(44):9770-9778.
• [61]Porter JT, Cauli B, Staiger JF, Lambolez B, Rossier J, Audinat E: Properties of bipolar VIPergic interneurons and their excitation by pyramidal neurons in the rat neocortex. Eur J Neurosci 1998, 10(12):3617-3628.
• [62]Caputi A, Rozov A, Blatow M, Monyer H: Two calretinin-positive GABAergic cell types in layer 2/3 of the mouse neocortex provide different forms of inhibition. Cereb Cortex 2009, 19(6):1345-1359.
• [63]Butt SJ, Fuccillo M, Nery S, Noctor S, Kriegstein A, Corbin JG, Fishell G: The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 2005, 48(4):591-604.
• [64]Kawaguchi Y, Kubota Y: Physiological and morphological identification of somatostatin- or vasoactive intestinal polypeptide-containing cells among GABAergic cell subtypes in rat frontal cortex. J Neurosci 1996, 16(8):2701-2715.
• [65]Olah S, Komlosi G, Szabadics J, Varga C, Toth E, Barzo P, Tamas G: Output of neurogliaform cells to various neuron types in the human and rat cerebral cortex. Front Neural Circ 2007, 1:4.
• [66]Price CJ, Cauli B, Kovacs ER, Kulik A, Lambolez B, Shigemoto R, Capogna M: Neurogliaform neurons form a novel inhibitory network in the hippocampal CA1 area. J Neurosci 2005, 25(29):6775-6786.
• [67]Simon A, Olah S, Molnar G, Szabadics J, Tamas G: Gap-junctional coupling between neurogliaform cells and various interneuron types in the neocortex. J Neurosci 2005, 25(27):6278-6285.
• [68]Zsiros V, Maccaferri G: Electrical coupling between interneurons with different excitable properties in the stratum lacunosum-moleculare of the juvenile CA1 rat hippocampus. J Neurosci 2005, 25(38):8686-8695.
• [69]Tamas G, Lorincz A, Simon A, Szabadics J: Identified sources and targets of slow inhibition in the neocortex. Science 2003, 299(5614):1902-1905.
• [70]Corbin JG, Butt SJ: Developmental mechanisms for the generation of telencephalic interneurons. Dev Neurobiol 2011, 71(8):710-732.
• [71]O’Rahilly R, Gardner E: The initial development of the human brain. Acta Anat 1979, 104(2):123-133.
• [72]Van Eden CG, Mrzljak L, Voorn P, Uylings HB: Prenatal development of GABA-ergic neurons in the neocortex of the rat. J Comp Neurol 1989, 289(2):213-227.
• [73]DeDiego I, Smith-Fernandez A, Fairen A: Cortical cells that migrate beyond area boundaries: characterization of an early neuronal population in the lower intermediate zone of prenatal rats. Eur J Neurosci 1994, 6(6):983-997.
• [74]de Carlos JA, Lopez-Mascaraque L, Valverde F: Dynamics of cell migration from the lateral ganglionic eminence in the rat. J Neurosci 1996, 16(19):6146-6156.
• [75]Tamamaki N, Fujimori KE, Takauji R: Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J Neurosci 1997, 17(21):8313-8323.
• [76]Mione MC, Danevic C, Boardman P, Harris B, Parnavelas JG: Lineage analysis reveals neurotransmitter (GABA or glutamate) but not calcium-binding protein homogeneity in clonally related cortical neurons. J Neurosci 1994, 14(1):107-123.
• [77]Parnavelas JG, Barfield JA, Franke E, Luskin MB: Separate progenitor cells give rise to pyramidal and nonpyramidal neurons in the rat telencephalon. Cereb Cortex 1991, 1(6):463-468.
• [78]Rakic P, Lombroso PJ: Development of the cerebral cortex: I. Forming the cortical structure. J Am Acad Child Adolesc Psychiatry 1998, 37(1):116-117.
• [79]Pleasure SJ, Anderson S, Hevner R, Bagri A, Marin O, Lowenstein DH, Rubenstein JL: Cell migration from the ganglionic eminences is required for the development of hippocampal GABAergic interneurons. Neuron 2000, 28(3):727-740.
• [80]Wonders CP, Anderson SA: The origin and specification of cortical interneurons. Nat Rev Neurosci 2006, 7(9):687-696.
• [81]Wonders CP, Taylor L, Welagen J, Mbata IC, Xiang JZ, Anderson SA: A spatial bias for the origins of interneuron subgroups within the medial ganglionic eminence. Dev Biol 2008, 314(1):127-136.
• [82]Xu Q, Cobos I, De La Cruz E, Rubenstein JL, Anderson SA: Origins of cortical interneuron subtypes. J Neurosci 2004, 24(11):2612-2622.
• [83]Cobos I, Calcagnotto ME, Vilaythong AJ, Thwin MT, Noebels JL, Baraban SC, Rubenstein JL: Mice lacking Dlx1 show subtype-specific loss of interneurons, reduced inhibition and epilepsy. Nat Neurosci 2005, 8(8):1059-1068.
• [84]Flames N, Pla R, Gelman DM, Rubenstein JL, Puelles L, Marin O: Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J Neurosci 2007, 27(36):9682-9695.
• [85]Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A: In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 2001, 128(19):3759-3771.
• [86]Corbin JG, Rutlin M, Gaiano N, Fishell G: Combinatorial function of the homeodomain proteins Nkx2.1 and Gsh2 in ventral telencephalic patterning. Development 2003, 130(20):4895-4906.
• [87]Anderson SA, Marin O, Horn C, Jennings K, Rubenstein JL: Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 2001, 128(3):353-363.
• [88]Nery S, Corbin JG, Fishell G: Dlx2 progenitor migration in wild type and Nkx2.1 mutant telencephalon. Cereb Cortex 2003, 13(9):895-903.
• [89]Nery S, Fishell G, Corbin JG: The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nat Neurosci 2002, 5(12):1279-1287.
• [90]Chameau P, Inta D, Vitalis T, Monyer H, Wadman WJ, van Hooft JA: The N-terminal region of reelin regulates postnatal dendritic maturation of cortical pyramidal neurons. Proc Natl Acad Sci U S A 2009, 106(17):7227-7232.
• [91]Inta D, Alfonso J, von Engelhardt J, Kreuzberg MM, Meyer AH, van Hooft JA, Monyer H: Neurogenesis and widespread forebrain migration of distinct GABAergic neurons from the postnatal subventricular zone. Proc Natl Acad Sci U S A 2008, 105(52):20994-20999.
• [92]Vucurovic K, Gallopin T, Ferezou I, Rancillac A, Chameau P, van Hooft JA, Geoffroy H, Monyer H, Rossier J, Vitalis T: Serotonin 3A receptor subtype as an early and protracted marker of cortical interneuron subpopulations. Cereb Cortex 2010, 20(10):2333-2347.
• [93]Gelman D, Griveau A, Dehorter N, Teissier A, Varela C, Pla R, Pierani A, Marin O: A wide diversity of cortical GABAergic interneurons derives from the embryonic preoptic area. J Neurosci 2011, 31(46):16570-16580.
• [94]Wichterle H, Garcia-Verdugo JM, Herrera DG, Alvarez-Buylla A: Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nat Neurosci 1999, 2(5):461-466.
• [95]Sussel L, Marin O, Kimura S, Rubenstein JL: Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 1999, 126(15):3359-3370.
• [96]Jimenez D, Lopez-Mascaraque LM, Valverde F, De Carlos JA: Tangential migration in neocortical development. Dev Biol 2002, 244(1):155-169.
• [97]Azim E, Jabaudon D, Fame RM, Macklis JD: SOX6 controls dorsal progenitor identity and interneuron diversity during neocortical development. Nat Neurosci 2009, 12(10):1238-1247.
• [98]Batista-Brito R, Rossignol E, Hjerling-Leffler J, Denaxa M, Wegner M, Lefebvre V, Pachnis V, Fishell G: The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 2009, 63(4):466-481.
• [99]Butt SJ, Sousa VH, Fuccillo MV, Hjerling-Leffler J, Miyoshi G, Kimura S, Fishell G: The requirement of Nkx2-1 in the temporal specification of cortical interneuron subtypes. Neuron 2008, 59(5):722-732.
• [100]Liodis P, Denaxa M, Grigoriou M, Akufo-Addo C, Yanagawa Y, Pachnis V: Lhx6 activity is required for the normal migration and specification of cortical interneuron subtypes. J Neurosci 2007, 27(12):3078-3089.
• [101]Wang Y, Dye CA, Sohal V, Long JE, Estrada RC, Roztocil T, Lufkin T, Deisseroth K, Baraban SC, Rubenstein JL: Dlx5 and Dlx6 regulate the development of parvalbumin-expressing cortical interneurons. J Neurosci 2010, 30(15):5334-5345.
• [102]Zhao Y, Flandin P, Long JE, Cuesta MD, Westphal H, Rubenstein JL: Distinct molecular pathways for development of telencephalic interneuron subtypes revealed through analysis of Lhx6 mutants. J Comp Neurol 2008, 510(1):79-99.
• [103]Fogarty M, Grist M, Gelman D, Marin O, Pachnis V, Kessaris N: Spatial genetic patterning of the embryonic neuroepithelium generates GABAergic interneuron diversity in the adult cortex. J Neurosci 2007, 27(41):10935-10946.
• [104]Xu Q, Tam M, Anderson SA: Fate mapping Nkx2.1-lineage cells in the mouse telencephalon. J Comp Neurol 2008, 506(1):16-29.
• [105]Xu Q, Wonders CP, Anderson SA: Sonic hedgehog maintains the identity of cortical interneuron progenitors in the ventral telencephalon. Development 2005, 132(22):4987-4998.
• [106]Xu Q, Guo L, Moore H, Waclaw RR, Campbell K, Anderson SA: Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 2010, 65(3):328-340.
• [107]Du T, Xu Q, Ocbina PJ, Anderson SA: NKX2.1 specifies cortical interneuron fate by activating Lhx6. Development 2008, 135(8):1559-1567.
• [108]Flandin P, Zhao Y, Vogt D, Jeong J, Long J, Potter G, Westphal H, Rubenstein JL: Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron 2011, 70(5):939-950.
• [109]Zhao Y, Marin O, Hermesz E, Powell A, Flames N, Palkovits M, Rubenstein JL, Westphal H: The LIM-homeobox gene Lhx8 is required for the development of many cholinergic neurons in the mouse forebrain. Proc Natl Acad Sci U S A 2003, 100(15):9005-9010.
• [110]Long JE, Cobos I, Potter GB, Rubenstein JL: Dlx1&2 and Mash1 transcription factors control MGE and CGE patterning and differentiation through parallel and overlapping pathways. Cereb Cortex 2009, 19(Suppl 1):i96-i106.
• [111]Long JE, Swan C, Liang WS, Cobos I, Potter GB, Rubenstein JL: Dlx1&2 and Mash1 transcription factors control striatal patterning and differentiation through parallel and overlapping pathways. J Comp Neurol 2009, 512(4):556-572.
• [112]Kanatani S, Yozu M, Tabata H, Nakajima K: COUP-TFII is preferentially expressed in the caudal ganglionic eminence and is involved in the caudal migratory stream. J Neurosci 2008, 28(50):13582-13591.
• [113]Willi-Monnerat S, Migliavacca E, Surdez D, Delorenzi M, Luthi-Carter R, Terskikh AV: Comprehensive spatiotemporal transcriptomic analyses of the ganglionic eminences demonstrate the uniqueness of its caudal subdivision. Mol Cell Neurosci 2008, 37(4):845-856.
• [114]Casarosa S, Fode C, Guillemot F: Mash1 regulates neurogenesis in the ventral telencephalon. Development 1999, 126(3):525-534.
• [115]Yun K, Fischman S, Johnson J, Hrabe de Angelis M, Weinmaster G, Rubenstein JL: Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 2002, 129(21):5029-5040.
• [116]Horton S, Meredith A, Richardson JA, Johnson JE: Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor MASH1. Mol Cell Neurosci 1999, 14(4–5):355-369.
• [117]Fode C, Ma Q, Casarosa S, Ang SL, Anderson DJ, Guillemot F: A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 2000, 14(1):67-80.
• [118]Toresson H, Potter SS, Campbell K: Genetic control of dorsal-ventral identity in the telencephalon: opposing roles for Pax6 and Gsh2. Development 2000, 127(20):4361-4371.
• [119]Yun K, Potter S, Rubenstein JL: Gsh2 and Pax6 play complementary roles in dorsoventral patterning of the mammalian telencephalon. Development 2001, 128(2):193-205.
• [120]Waclaw RR, Wang B, Pei Z, Ehrman LA, Campbell K: Distinct temporal requirements for the homeobox gene Gsx2 in specifying striatal and olfactory bulb neuronal fates. Neuron 2009, 63(4):451-465.
• [121]Panganiban G, Rubenstein JL: Developmental functions of the distal-less/Dlx homeobox genes. Development 2002, 129(19):4371-4386.
• [122]Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles L, Rubenstein JL: DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 1999, 414(2):217-237.
• [123]Liu JK, Ghattas I, Liu S, Chen S, Rubenstein JL: Dlx genes encode DNA-binding proteins that are expressed in an overlapping and sequential pattern during basal ganglia differentiation. Dev Dyn 1997, 210(4):498-512.
• [124]Anderson SA, Eisenstat DD, Shi L, Rubenstein JL: Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 1997, 278(5337):474-476.
• [125]Gelman DM, Marin O, Rubenstein JLR: The Generation of Cortical Interneurons. In Jasper’s Basic Mechanisms of the Epilepsies. 4th edition. Edited by Noebels JL, Avoli M, Rogawski MA, Olsen RW, Delgado-Escueta AV. Bethesda (MD); 2012.
• [126]Gelman DM, Martini FJ, Nobrega-Pereira S, Pierani A, Kessaris N, Marin O: The embryonic preoptic area is a novel source of cortical GABAergic interneurons. J Neurosci 2009, 29(29):9380-9389.
• [127]Lodato S, Rouaux C, Quast KB, Jantrachotechatchawan C, Studer M, Hensch TK, Arlotta P: Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 2011, 69(4):763-779.
• [128]Sugiyama S, Di Nardo AA, Aizawa S, Matsuo I, Volovitch M, Prochiantz A, Hensch TK: Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 2008, 134(3):508-520.
• [129]Beurdeley M, Spatazza J, Lee HH, Sugiyama S, Bernard C, Di Nardo AA, Hensch TK, Prochiantz A: Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J Neurosci 2012, 32(27):9429-9437.
• [130]Petanjek Z, Kostovic I, Esclapez M: Primate-specific origins and migration of cortical GABAergic neurons. Front Neuroanat 2009, 3:26.
• [131]Letinic K, Zoncu R, Rakic P: Origin of GABAergic neurons in the human neocortex. Nature 2002, 417(6889):645-649.
• [132]Yu X, Zecevic N: Dorsal radial glial cells have the potential to generate cortical interneurons in human but not in mouse brain. J Neurosci 2011, 31(7):2413-2420.
• [133]Fertuzinhos S, Krsnik Z, Kawasawa YI, Rasin MR, Kwan KY, Chen JG, Judas M, Hayashi M, Sestan N: Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia. Cereb Cortex 2009, 19(9):2196-2207.
• [134]Petanjek Z, Berger B, Esclapez M: Origins of cortical GABAergic neurons in the cynomolgus monkey. Cereb Cortex 2009, 19(2):249-262.
• [135]Rakic S, Zecevic N: Early oligodendrocyte progenitor cells in the human fetal telencephalon. Glia 2003, 41(2):117-127.
• [136]Zecevic N, Hu F, Jakovcevski I: Interneurons in the developing human neocortex. Dev Neurobiol 2011, 71(1):18-33.
• [137]Jakovcevski I, Mayer N, Zecevic N: Multiple origins of human neocortical interneurons are supported by distinct expression of transcription factors. Cereb Cortex 2011, 21(8):1771-1782.
• [138]Tanaka DH, Oiwa R, Sasaki E, Nakajima K: Changes in cortical interneuron migration contribute to the evolution of the neocortex. Proc Natl Acad Sci U S A 2011, 108(19):8015-8020.
• [139]Corbin JG, Nery S, Fishell G: Telencephalic cells take a tangent: non-radial migration in the mammalian forebrain. Nat Neurosci 2001, 4(Suppl):1177-1182.
• [140]Marin O, Rubenstein JL: A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci 2001, 2(11):780-790.
• [141]Marin O, Rubenstein JL: Cell migration in the forebrain. Annu Rev Neurosci 2003, 26:441-483.
• [142]Metin C, Baudoin JP, Rakic S, Parnavelas JG: Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 2006, 23(4):894-900.
• [143]Lavdas AA, Grigoriou M, Pachnis V, Parnavelas JG: The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J Neurosci 1999, 19(18):7881-7888.
• [144]Faux C, Rakic S, Andrews W, Yanagawa Y, Obata K, Parnavelas JG: Differential gene expression in migrating cortical interneurons during mouse forebrain development. J Comp Neurol 2010, 518(8):1232-1248.
• [145]Marsh ED, Minarcik J, Campbell K, Brooks-Kayal AR, Golden JA: FACS-array gene expression analysis during early development of mouse telencephalic interneurons. Dev Neurobiol 2008, 68(4):434-445.
• [146]Powell EM, Mars WM, Levitt P: Hepatocyte growth factor/scatter factor is a motogen for interneurons migrating from the ventral to dorsal telencephalon. Neuron 2001, 30(1):79-89.
• [147]Powell EM, Campbell DB, Stanwood GD, Davis C, Noebels JL, Levitt P: Genetic disruption of cortical interneuron development causes region- and GABA cell type-specific deficits, epilepsy, and behavioral dysfunction. J Neurosci 2003, 23(2):622-631.
• [148]Friedman WJ, Black IB, Kaplan DR: Distribution of the neurotrophins brain-derived neurotrophic factor, neurotrophin-3, and neurotrophin-4/5 in the postnatal rat brain: an immunocytochemical study. Neuroscience 1998, 84(1):101-114.
• [149]Fukumitsu H, Furukawa Y, Tsusaka M, Kinukawa H, Nitta A, Nomoto H, Mima T, Furukawa S: Simultaneous expression of brain-derived neurotrophic factor and neurotrophin-3 in Cajal-Retzius, subplate and ventricular progenitor cells during early development stages of the rat cerebral cortex. Neuroscience 1998, 84(1):115-127.
• [150]Maisonpierre PC, Belluscio L, Friedman B, Alderson RF, Wiegand SJ, Furth ME, Lindsay RM, Yancopoulos GD: NT-3, BDNF, and NGF in the developing rat nervous system: parallel as well as reciprocal patterns of expression. Neuron 1990, 5(4):501-509.
• [151]Timmusk T, Belluardo N, Metsis M, Persson H: Widespread and developmentally regulated expression of neurotrophin-4 mRNA in rat brain and peripheral tissues. Eur J Neurosci 1993, 5(6):605-613.
• [152]Gorba T, Wahle P: Expression of TrkB and TrkC but not BDNF mRNA in neurochemically identified interneurons in rat visual cortex in vivo and in organotypic cultures. Eur J Neurosci 1999, 11(4):1179-1190.
• [153]Klein R, Martin-Zanca D, Barbacid M, Parada LF: Expression of the tyrosine kinase receptor gene trkB is confined to the murine embryonic and adult nervous system. Development 1990, 109(4):845-850.
• [154]Brunstrom JE, Gray-Swain MR, Osborne PA, Pearlman AL: Neuronal heterotopias in the developing cerebral cortex produced by neurotrophin-4. Neuron 1997, 18(3):505-517.
• [155]Fiumelli H, Kiraly M, Ambrus A, Magistretti PJ, Martin JL: Opposite regulation of calbindin and calretinin expression by brain-derived neurotrophic factor in cortical neurons. J Neurochem 2000, 74(5):1870-1877.
• [156]Arenas E, Akerud P, Wong V, Boylan C, Persson H, Lindsay RM, Altar CA: Effects of BDNF and NT-4/5 on striatonigral neuropeptides or nigral GABA neurons in vivo. Eur J Neurosci 1996, 8(8):1707-1717.
• [157]Jones KR, Farinas I, Backus C, Reichardt LF: Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 1994, 76(6):989-999.
• [158]Pozas E, Ibanez CF: GDNF and GFRalpha1 promote differentiation and tangential migration of cortical GABAergic neurons. Neuron 2005, 45(5):701-713.
• [159]Airaksinen MS, Saarma M: The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 2002, 3(5):383-394.
• [160]Canty AJ, Dietze J, Harvey M, Enomoto H, Milbrandt J, Ibanez CF: Regionalized loss of parvalbumin interneurons in the cerebral cortex of mice with deficits in GFRalpha1 signaling. J Neurosci 2009, 29(34):10695-10705.
• [161]Wichterle H, Alvarez-Dolado M, Erskine L, Alvarez-Buylla A: Permissive corridor and diffusible gradients direct medial ganglionic eminence cell migration to the neocortex. Proc Natl Acad Sci U S A 2003, 100(2):727-732.
• [162]Marin O, Yaron A, Bagri A, Tessier-Lavigne M, Rubenstein JL: Sorting of striatal and cortical interneurons regulated by semaphorin-neuropilin interactions. Science 2001, 293(5531):872-875.
• [163]Tamamaki N, Fujimori K, Nojyo Y, Kaneko T, Takauji R: Evidence that Sema3A and Sema3F regulate the migration of GABAergic neurons in the developing neocortex. J Comp Neurol 2003, 455(2):238-248.
• [164]Zimmer G, Schanuel SM, Burger S, Weth F, Steinecke A, Bolz J, Lent R: Chondroitin sulfate acts in concert with semaphorin 3A to guide tangential migration of cortical interneurons in the ventral telencephalon. Cereb Cortex 2010, 20(10):2411-2422.
• [165]Bagri A, Marin O, Plump AS, Mak J, Pleasure SJ, Rubenstein JL, Tessier-Lavigne M: Slit proteins prevent midline crossing and determine the dorsoventral position of major axonal pathways in the mammalian forebrain. Neuron 2002, 33(2):233-248.
• [166]Marillat V, Cases O, Nguyen-Ba-Charvet KT, Tessier-Lavigne M, Sotelo C, Chedotal A: Spatiotemporal expression patterns of slit and robo genes in the rat brain. J Comp Neurol 2002, 442(2):130-155.
• [167]Whitford KL, Marillat V, Stein E, Goodman CS, Tessier-Lavigne M, Chedotal A, Ghosh A: Regulation of cortical dendrite development by slit-robo interactions. Neuron 2002, 33(1):47-61.
• [168]Yuan W, Zhou L, Chen JH, Wu JY, Rao Y, Ornitz DM: The mouse SLIT family: secreted ligands for ROBO expressed in patterns that suggest a role in morphogenesis and axon guidance. Dev Biol 1999, 212(2):290-306.
• [169]Andrews W, Barber M, Hernadez-Miranda LR, Xian J, Rakic S, Sundaresan V, Rabbitts TH, Pannell R, Rabbitts P, Thompson H: The role of slit-robo signaling in the generation, migration and morphological differentiation of cortical interneurons. Dev Biol 2008, 313(2):648-658.
• [170]Andrews W, Liapi A, Plachez C, Camurri L, Zhang J, Mori S, Murakami F, Parnavelas JG, Sundaresan V, Richards LJ: Robo1 regulates the development of major axon tracts and interneuron migration in the forebrain. Development 2006, 133(11):2243-2252.
• [171]Andrews WD, Barber M, Parnavelas JG: Slit-robo interactions during cortical development. J Anat 2007, 211(2):188-198.
• [172]Barber M, Di Meglio T, Andrews WD, Hernandez-Miranda LR, Murakami F, Chedotal A, Parnavelas JG: The role of Robo3 in the development of cortical interneurons. Cereb Cortex 2009, 19(Suppl 1):i22-i31.
• [173]Zimmer G, Garcez P, Rudolph J, Niehage R, Weth F, Lent R, Bolz J: Ephrin-A5 acts as a repulsive cue for migrating cortical interneurons. Eur J Neurosci 2008, 28(1):62-73.
• [174]Rudolph J, Zimmer G, Steinecke A, Barchmann S, Bolz J: Ephrins guide migrating cortical interneurons in the basal telencephalon. Cell Adh Migr 2010, 4(3):400-408.
• [175]Sanchez-Alcaniz JA, Haege S, Mueller W, Pla R, Mackay F, Schulz S, Lopez-Bendito G, Stumm R, Marin O: Cxcr7 controls neuronal migration by regulating chemokine responsiveness. Neuron 2011, 69(1):77-90.
• [176]Tiveron MC, Rossel M, Moepps B, Zhang YL, Seidenfaden R, Favor J, Konig N, Cremer H: Molecular interaction between projection neuron precursors and invading interneurons via stromal-derived factor 1 (CXCL12)/CXCR4 signaling in the cortical subventricular zone/intermediate zone. J Neurosci 2006, 26(51):13273-13278.
• [177]Li G, Adesnik H, Li J, Long J, Nicoll RA, Rubenstein JL, Pleasure SJ: Regional distribution of cortical interneurons and development of inhibitory tone are regulated by Cxcl12/Cxcr4 signaling. J Neurosci 2008, 28(5):1085-1098.
• [178]Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marin O: Short- and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 2004, 44(2):251-261.
• [179]Martini FJ, Valiente M, Lopez Bendito G, Szabo G, Moya F, Valdeolmillos M, Marin O: Biased selection of leading process branches mediates chemotaxis during tangential neuronal migration. Development 2009, 136(1):41-50.
• [180]Yau HJ, Wang HF, Lai C, Liu FC: Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences. Cereb Cortex 2003, 13(3):252-264.
• [181]Gong S, Zheng C, Doughty ML, Losos K, Didkovsky N, Schambra UB, Nowak NJ, Joyner A, Leblanc G, Hatten ME: A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425(6961):917-925.
• [182]Alifragis P, Liapi A, Parnavelas JG: Lhx6 regulates the migration of cortical interneurons from the ventral telencephalon but does not specify their GABA phenotype. J Neurosci 2004, 24(24):5643-5648.
• [183]Nobrega-Pereira S, Kessaris N, Du T, Kimura S, Anderson SA, Marin O: Postmitotic Nkx2-1 controls the migration of telencephalic interneurons by direct repression of guidance receptors. Neuron 2008, 59(5):733-745.
• [184]Cobos I, Borello U, Rubenstein JL: Dlx transcription factors promote migration through repression of axon and dendrite growth. Neuron 2007, 54(6):873-888.
• [185]Cobos I, Broccoli V, Rubenstein JL: The vertebrate ortholog of Aristaless is regulated by Dlx genes in the developing forebrain. J Comp Neurol 2005, 483(3):292-303.
• [186]Colombo E, Collombat P, Colasante G, Bianchi M, Long J, Mansouri A, Rubenstein JL, Broccoli V: Inactivation of Arx, the murine ortholog of the X-linked lissencephaly with ambiguous genitalia gene, leads to severe disorganization of the ventral telencephalon with impaired neuronal migration and differentiation. J Neurosci 2007, 27(17):4786-4798.
• [187]Kitamura K, Yanazawa M, Sugiyama N, Miura H, Iizuka-Kogo A, Kusaka M, Omichi K, Suzuki R, Kato-Fukui Y, Kamiirisa K: Mutation of ARX causes abnormal development of forebrain and testes in mice and X-linked lissencephaly with abnormal genitalia in humans. Nat Genet 2002, 32(3):359-369.
• [188]Marsh E, Fulp C, Gomez E, Nasrallah I, Minarcik J, Sudi J, Christian SL, Mancini G, Labosky P, Dobyns W: Targeted loss of Arx results in a developmental epilepsy mouse model and recapitulates the human phenotype in heterozygous females. Brain 2009, 132(Pt 6):1563-1576.
• [189]Cuzon VC, Yeh PW, Cheng Q, Yeh HH: Ambient GABA promotes cortical entry of tangentially migrating cells derived from the medial ganglionic eminence. Cereb Cortex 2006, 16(10):1377-1388.
• [190]Lopez-Bendito G, Lujan R, Shigemoto R, Ganter P, Paulsen O, Molnar Z: Blockade of GABA(B) receptors alters the tangential migration of cortical neurons. Cereb Cortex 2003, 13(9):932-942.
• [191]Cuzon Carlson VC, Yeh HH: GABAA receptor subunit profiles of tangentially migrating neurons derived from the medial ganglionic eminence. Cereb Cortex 2011, 21(8):1792-1802.
• [192]Crandall JE, McCarthy DM, Araki KY, Sims JR, Ren JQ, Bhide PG: Dopamine receptor activation modulates GABA neuron migration from the basal forebrain to the cerebral cortex. J Neurosci 2007, 27(14):3813-3822.
• [193]Ohtani N, Goto T, Waeber C, Bhide PG: Dopamine modulates cell cycle in the lateral ganglionic eminence. J Neurosci 2003, 23(7):2840-2850.
• [194]Sahara S, Yanagawa Y, O’Leary DD, Stevens CF: The fraction of cortical GABAergic neurons is constant from near the start of cortical neurogenesis to adulthood. J Neurosci 2012, 32(14):4755-4761.
• [195]Faux C, Rakic S, Andrews W, Britto JM: Neurons on the move: migration and lamination of cortical interneurons. Neurosignals 2012, 20(3):168-189.
• [196]Bortone D, Polleux F: KCC2 expression promotes the termination of cortical interneuron migration in a voltage-sensitive calcium-dependent manner. Neuron 2009, 62(1):53-71.
• [197]Elvevag B, Goldberg TE: Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 2000, 14(1):1-21.
• [198]Sitskoorn MM, Aleman A, Ebisch SJ, Appels MC, Kahn RS: Cognitive deficits in relatives of patients with schizophrenia: a meta-analysis. Schizophr Res 2004, 71(2–3):285-295.
• [199]Benes FM, McSparren J, Bird ED, SanGiovanni JP, Vincent SL: Deficits in small interneurons in prefrontal and cingulate cortices of schizophrenic and schizoaffective patients. Arch Gen Psychiatry 1991, 48(11):996-1001.
• [200]Akbarian S, Kim JJ, Potkin SG, Hagman JO, Tafazzoli A, Bunney WE Jr, Jones EG: Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch Gen Psychiatry 1995, 52(4):258-266.
• [201]Hashimoto T, Volk DW, Eggan SM, Mirnics K, Pierri JN, Sun Z, Sampson AR, Lewis DA: Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J Neurosci 2003, 23(15):6315-6326.
• [202]Lewis DA, Sweet RA: Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. J Clin Invest 2009, 119(4):706-716.
• [203]Lisman JE, Coyle JT, Green RW, Javitt DC, Benes FM, Heckers S, Grace AA: Circuit-based framework for understanding neurotransmitter and risk gene interactions in schizophrenia. Trends Neurosci 2008, 31(5):234-242.
• [204]Barr MS, Farzan F, Tran LC, Chen R, Fitzgerald PB, Daskalakis ZJ: Evidence for excessive frontal evoked gamma oscillatory activity in schizophrenia during working memory. Schizophr Res 2010, 121(1–3):146-152.
• [205]Farzan F, Barr MS, Levinson AJ, Chen R, Wong W, Fitzgerald PB, Daskalakis ZJ: Evidence for gamma inhibition deficits in the dorsolateral prefrontal cortex of patients with schizophrenia. Brain 2010, 133(Pt 5):1505-1514.
• [206]Haenschel C, Bittner RA, Waltz J, Haertling F, Wibral M, Singer W, Linden DE, Rodriguez E: Cortical oscillatory activity is critical for working memory as revealed by deficits in early-onset schizophrenia. J Neurosci 2009, 29(30):9481-9489.
• [207]Uhlhaas PJ, Singer W: Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 2010, 11(2):100-113.
• [208]Stefansson H, Sarginson J, Kong A, Yates P, Steinthorsdottir V, Gudfinnsson E, Gunnarsdottir S, Walker N, Petursson H, Crombie C: Association of neuregulin 1 with schizophrenia confirmed in a Scottish population. Am J Hum Genet 2003, 72(1):83-87.
• [209]Harrison PJ, Law AJ: Neuregulin 1 and schizophrenia: genetics, gene expression, and neurobiology. Biol Psychiatry 2006, 60(2):132-140.
• [210]Wen L, Lu YS, Zhu XH, Li XM, Woo RS, Chen YJ, Yin DM, Lai C, Terry AV Jr, Vazdarjanova A: Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 2010, 107(3):1211-1216.
• [211]Mei L, Xiong WC: Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 2008, 9(6):437-452.
• [212]Fazzari P, Paternain AV, Valiente M, Pla R, Lujan R, Lloyd K, Lerma J, Marin O, Rico B: Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 2010, 464(7293):1376-1380.
• [213]Vullhorst D, Neddens J, Karavanova I, Tricoire L, Petralia RS, McBain CJ, Buonanno A: Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 2009, 29(39):12255-12264.
• [214]Millar JK, Wilson-Annan JC, Anderson S, Christie S, Taylor MS, Semple CA, Devon RS, St Clair DM, Muir WJ, Blackwood DH: Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 2000, 9(9):1415-1423.
• [215]Hikida T, Jaaro-Peled H, Seshadri S, Oishi K, Hookway C, Kong S, Wu D, Xue R, Andrade M, Tankou S: Dominant-negative DISC1 transgenic mice display schizophrenia-associated phenotypes detected by measures translatable to humans. Proc Natl Acad Sci U S A 2007, 104(36):14501-14506.
• [216]Niwa M, Kamiya A, Murai R, Kubo K, Gruber AJ, Tomita K, Lu L, Tomisato S, Jaaro-Peled H, Seshadri S: Knockdown of DISC1 by in utero gene transfer disturbs postnatal dopaminergic maturation in the frontal cortex and leads to adult behavioral deficits. Neuron 2010, 65(4):480-489.
• [217]Porteous DJ, Millar JK, Brandon NJ, Sawa A: DISC1 at 10: connecting psychiatric genetics and neuroscience. Trends Mol Med 2011, 17(12):699-706.
• [218]Ji Y, Yang F, Papaleo F, Wang HX, Gao WJ, Weinberger DR, Lu B: Role of dysbindin in dopamine receptor trafficking and cortical GABA function. Proc Natl Acad Sci U S A 2009, 106(46):19593-19598.
• [219]Straub RE, Jiang Y, MacLean CJ, Ma Y, Webb BT, Myakishev MV, Harris-Kerr C, Wormley B, Sadek H, Kadambi B: Genetic variation in the 6p22.3 gene DTNBP1, the human ortholog of the mouse dysbindin gene, is associated with schizophrenia. Am J Hum Genet 2002, 71(2):337-348.
• [220]Talbot K, Eidem WL, Tinsley CL, Benson MA, Thompson EW, Smith RJ, Hahn CG, Siegel SJ, Trojanowski JQ, Gur RE: Dysbindin-1 is reduced in intrinsic, glutamatergic terminals of the hippocampal formation in schizophrenia. J Clin Invest 2004, 113(9):1353-1363.
• [221]Weickert CS, Straub RE, McClintock BW, Matsumoto M, Hashimoto R, Hyde TM, Herman MM, Weinberger DR, Kleinman JE: Human dysbindin (DTNBP1) gene expression in normal brain and in schizophrenic prefrontal cortex and midbrain. Arch Gen Psychiatry 2004, 61(6):544-555.
• [222]Ottis P, Bader V, Trossbach SV, Kretzschmar H, Michel M, Leliveld SR, Korth C: Convergence of two independent mental disease genes on the protein level: recruitment of dysbindin to cell-invasive disrupted-in-schizophrenia 1 aggresomes. Biol Psychiatry 2011, 70(7):604-610.