Development of GABA circuitry of fast-spiking basket interneurons in the medial prefrontal cortex of erbb4-mutant mice

Journal of Neuroscience

Volumn 33, Issue 50, 2013, Pages 19724-19733

  Yang, Jian Ming ^a   Zhang, Jing ^a   Chen, Xiao Juan ^a   Geng, Hong Yan ^a   Ye, Mao ^a   Spitzer, Nicholas C ^b   Luo, Jian Hong ^a,c   Duan, Shu Min ^a,c   Li, Xiao Ming ^a,c  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Development; ErbB4; GABAergic circuitry; Medial prefrontal cortex (mPFC); Parvalbumin (PV) interneurons; Schizophrenia

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; BETA ACTIN; EPIDERMAL GROWTH FACTOR RECEPTOR 4; GEPHYRIN; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; NEURON SPECIFIC NUCLEAR PROTEIN; PARVALBUMIN; PROTEIN KINASE B;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN ELECTROPHYSIOLOGY; BRAIN MATURATION; CONTROLLED STUDY; EVOKED RESPONSE; FLUORESCENCE MICROSCOPY; FOREBRAIN; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; SCHIZOPHRENIA; SYNAPSE; SYNAPTOGENESIS; WESTERN BLOTTING;

DEVELOPMENT; ERBB4; GABAERGIC CIRCUITRY; MEDIAL PREFRONTAL CORTEX (MPFC); PARVALBUMIN (PV) INTERNEURONS; SCHIZOPHRENIA;

ANIMALS; GAMMA-AMINOBUTYRIC ACID; INTERNEURONS; MICE; MICE, KNOCKOUT; NERVE NET; PARVALBUMINS; PREFRONTAL CORTEX; PYRAMIDAL CELLS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84889799561     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1584-13.2013     Document Type: Article

References (46)

1. Abe Y, Namba H, Kato T, Iwakura Y, Nawa H (2011) Neuregulin-1 signals from the periphery regulate AMPA receptor sensitivity and expression in GABAergic interneurons in developing neocortex. J Neurosci 31:5699-5709. CrossRef Medline
2. Barros CS, Calabrese B, Chamero P, Roberts AJ, Korzus E, Lloyd K, Stowers L, Mayford M, Halpain S, Müller U (2009) Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Proc Natl Acad Sci U S A 106:4507-4512. CrossRef Medline
3. Belforte JE, Zsiros V, Sklar ER, Jiang Z, Yu G, Li Y, Quinlan EM, Nakazawa K (2010) PostnatalNMDAreceptor ablation in corticolimbic interneurons confers schizophrenia-like phenotypes. Nat Neurosci 13:76-83. CrossRef Medline
4. Bennett MV, Zukin RS (2004) Electrical coupling and neuronal synchronization in the mammalian brain. Neuron 41:495-511. CrossRef Medline
5. Callicott JH, Mattay VS, Verchinski BA, Marenco S, Egan MF, Weinberger DR (2003) Complexity of prefrontal cortical dysfunction in schizophrenia: more than up or down. Am J Psychiatry 160:2209-2215. CrossRef Medline
6. Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611. CrossRef Medline
7. Chen YJ, Zhang M, Yin DM, Wen L, Ting A, Wang P, Lu YS, Zhu XH, Li SJ, Wu CY, Wang XM, Lai C, Xiong WC, Mei L, Gao TM (2010) ErbB4 in parvalbumin-positive interneurons is critical for neuregulin 1 regulation of long-term potentiation. Proc Natl Acad Sci U S A 107:21818-21823. CrossRef Medline
8. Cooper MA, Koleske AJ (2011) ErbB4 localization to interneurons: clearer insights into schizophrenia pathology. Biol Psychiatry 70:602-603. CrossRef Medline
9. Fazzari P, Paternain AV, Valiente M, Pla R, Luján R, Lloyd K, Lerma J, Marín O, Rico B (2010) Control of cortical GABA circuitry development by Nrg1 and ErbB4 signalling. Nature 464:1376-1380. CrossRef Medline
10. Fisahn A, Neddens J, Yan L, Buonanno A (2009) Neuregulin-1 modulates hippocampal gamma oscillations: implications for schizophrenia. Cereb Cortex 19:612-618. CrossRef Medline
11. Flames N, Long JE, Garratt AN, Fischer TM, Gassmann M, Birchmeier C, Lai C, Rubenstein JL, Marín O (2004) Short-and long-range attraction of cortical GABAergic interneurons by neuregulin-1. Neuron 44:251-261. CrossRef Medline
12. Fuchs EC, Zivkovic AR, Cunningham MO, Middleton S, Lebeau FE, Bannerman DM, Rozov A, Whittington MA, Traub RD, Rawlins JN, Monyer H (2007) Recruitment of parvalbumin-positive interneurons determines hippocampal function and associated behavior. Neuron 53:591-604. CrossRef Medline
13. Gajendran N, Kapfhammer JP, Lain E, Canepari M, Vogt K, Wisden W, BrennerHR (2009) Neuregulin signaling is dispensable forNMDA-and GABA(A)-receptor expression in the cerebellum in vivo. J Neurosci 29: 2404-2413. CrossRef Medline
14. Garcia RA, Vasudevan K, Buonanno A (2000) The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc Natl Acad Sci U S A 97:3596-3601. CrossRef Medline
15. Gu Z, Jiang Q, Fu AK, Ip NY, Yan Z (2005) Regulation of NMDA receptors by neuregulin signaling in prefrontal cortex. J Neurosci 25:4974-4984. CrossRef Medline
16. Huang YZ, Won S, Ali DW, Wang Q, Tanowitz M, Du QS, Pelkey KA, Yang DJ, Xiong WC, Salter MW, Mei L (2000) Regulation of neuregulin signaling by PSD-95 interacting with ErbB4 at CNS synapses. Neuron 26: 443-455. CrossRef Medline
17. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638-2655. Medline
18. Kawaguchi Y, Kubota Y (1997) GABAergic cell subtypes and their synaptic connections in rat frontal cortex. Cereb Cortex 7:476-486. CrossRef Medline
19. Korotkova T, Fuchs EC, Ponomarenko A, von Engelhardt J, Monyer H (2010) NMDA receptor ablation on parvalbumin-positive interneurons impairs hippocampal synchrony, spatial representations, and working memory. Neuron 68:557-569. CrossRef Medline
20. Krivosheya D, Tapia L, Levinson JN, Huang K, Kang Y, Hines R, Ting AK, Craig AM, Mei L, Bamji SX, El-Husseini A (2008) ErbB4-neuregulin signaling modulates synapse development and dendritic arborization through distinct mechanisms. J Biol Chem 283:32944-32956. CrossRef Medline
21. Lewis DA, González-Burgos G (2008) Neuroplasticity of neocortical circuits in schizophrenia. Neuropsychopharmacology 33:141-165. CrossRef Medline
22. Lewis DA, Hashimoto T, Volk DW (2005) Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6:312-324. CrossRef Medline
23. Li B, Woo RS, Mei L, Malinow R (2007) The neuregulin-1 receptor erbB4 controls glutamatergic synapse maturation and plasticity. Neuron 54: 583-597. CrossRef Medline
24. Li H, Chou SJ, Hamasaki T, Perez-Garcia CG, O'Leary DD (2012a) Neuregulin repellent signaling via ErbB4 restricts GABAergic interneurons to migratory paths from ganglionic eminence to cortical destinations. Neural Dev 7:10. CrossRef Medline
25. Li KX, Lu YM, Xu ZH, Zhang J, Zhu JM, Zhang JM, Cao SX, Chen XJ, Chen Z, Luo JH, Duan S, LiXM (2012b) Neuregulin 1 regulates excitability of fast-spiking neurons through Kv1.1 and acts in epilepsy. Nat Neurosci 15:267-273. CrossRef Medline
26. Marín O (2012) Interneuron dysfunction in psychiatric disorders. Nat Rev Neurosci 13:107-120. CrossRef Medline
27. Mei L, Xiong WC (2008) Neuregulin 1 in neural development, synaptic plasticity and schizophrenia. Nat Rev Neurosci 9:437-452. CrossRef Medline
28. Neddens J, Buonanno A (2010) Selective populations of hippocampal interneurons express ErbB4 and their number and distribution is altered in ErbB4 knockout mice. Hippocampus 20:724-744. CrossRef Medline
29. Neddens J, Fish KN, Tricoire L, Vullhorst D, Shamir A, Chung W, Lewis DA, McBain CJ, Buonanno A (2011) Conserved interneuron-specific ErbB4 expression in frontal cortex of rodents, monkeys, and humans: implications for schizophrenia. Biol Psychiatry 70:636-645. CrossRef Medline
30. Rio C, Rieff HI, Qi P, Khurana TS, Corfas G (1997) Neuregulin and erbB receptors play a critical role in neuronal migration. Neuron 19:39-50. CrossRef Medline
31. Shamir A, Kwon OB, Karavanova I, Vullhorst D, Leiva-Salcedo E, Janssen MJ, Buonanno A (2012) The importance of the NRG-1/ErbB4 pathway for synaptic plasticity and behaviors associated with psychiatric disorders. J Neurosci 32:2988-2997. CrossRef Medline
32. Shimamura K, Martinez S, Puelles L, Rubenstein JL (1997) Patterns of gene expression in the neural plate and neural tube subdivide the embryonic forebrain into transverse and longitudinal domains. Dev Neurosci 19:88-96. CrossRef Medline
33. Silberberg G, Darvasi A, Pinkas-Kramarski R, Navon R (2006) The involvement of ErbB4 with schizophrenia: association and expression studies. Am J Med Genet B Neuropsychiatr Genet 141B:142-148. CrossRef Medline
34. Soltesz I, Smetters DK, Mody I (1995) Tonic inhibition originates from synapses close to the soma. Neuron 14:1273-1283. CrossRef Medline
35. Tan GH, Liu YY, Hu XL, Yin DM, Mei L, Xiong ZQ (2012) Neuregulin 1 represses limbic epileptogenesis through ErbB4 in parvalbuminexpressing interneurons. Nat Neurosci 15:258-266. CrossRef Medline
36. Taniguchi H, Lu J, Huang ZJ (2013) The spatial and temporal origin of chandelier cells in mouse neocortex. Science 339:70-74. CrossRef Medline
37. Ting AK, Chen Y, Wen L, Yin DM, Shen C, Tao Y, Liu X, Xiong WC, Mei L (2011) Neuregulin 1 promotes excitatory synapse development and function in GABAergic interneurons. J Neurosci 31:15-25. CrossRef Medline
38. Turrigiano GG, Nelson SB (2004) Homeostatic plasticity in the developing nervous system. Nat Rev Neurosci 5:97-107. CrossRef Medline
39. Vullhorst D, Neddens J, Karavanova I, Tricoire L, Petralia RS, McBain CJ, Buonanno A (2009) Selective expression of ErbB4 in interneurons, but not pyramidal cells, of the rodent hippocampus. J Neurosci 29:12255-12264. CrossRef Medline
40. Wen L, Lu YS, Zhu XH, Li XM, Woo RS, Chen YJ, Yin DM, Lai C, Terry AV Jr, Vazdarjanova A, Xiong WC, Mei L (2010) Neuregulin 1 regulates pyramidal neuron activity via ErbB4 in parvalbumin-positive interneurons. Proc Natl Acad Sci U S A 107:1211-1216. CrossRef Medline
41. Williams SM, Goldman-Rakic PS, Leranth C (1992) The synaptology of parvalbumin-immunoreactive neurons in the primate prefrontal cortex. J Comp Neurol 320:353-369. CrossRef Medline
42. Woo RS, Li XM, Tao Y, Carpenter-Hyland E, Huang YZ, Weber J, Neiswender H, Dong XP, WuJ, Gassmann M, Lai C, Xiong WC, Gao TM, Mei L (2007) Neuregulin-1 enhances depolarization-induced GABA release. Neuron 54:599-610. CrossRef Medline
43. Yang JM, Zhang J, Yu YQ, Duan S, Li XM (2012) Postnatal development of 2 microcircuits involving fast-spiking interneurons in the mouse prefrontal cortex. Cereb Cortex, in press. CrossRef Medline
44. Yau HJ, Wang HF, Lai C, Liu FC (2003) 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 13:252-264. CrossRef Medline
45. Yizhar O, Fenno LE, Prigge M, Schneider F, Davidson TJ, O'Shea DJ, Sohal VS, Goshen I, Finkelstein J, Paz JT, Stehfest K, Fudim R, Ramakrishnan C, Huguenard JR, Hegemann P, Deisseroth K (2011) Neocortical excitation/ inhibition balance in information processing and social dysfunction. Nature 477:171-178. CrossRef Medline
46. Zerucha T, Stühmer T, Hatch G, Park BK, Long Q, Yu G, Gambarotta A, Schultz JR, Rubenstein JL, EkkerM (2000) A highly conserved enhancer in the Dlx5/Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx genes in the embryonic forebrain. J Neurosci 20:709-721. Medline