Electrical excitability of early neurons in the human cerebral cortex during the second trimester of gestation

Cerebral Cortex

Volumn 19, Issue 8, 2009, Pages 1795-1805

  Moore, Anna R ^a   Filipovic, Radmila ^a   Mo, Zhicheng ^a   Rasband, Matthew N ^b   Zecevic, Nada ^a   Antic, Srdjan D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Action potential; Axon initial segment; Cortical plate; Sodium current; Subplate; Subventricular zone

Indexed keywords

SODIUM; SPECTRIN; TETRODOTOXIN; VOLTAGE GATED SODIUM CHANNEL;

ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; FETUS; HUMAN; HUMAN TISSUE; NERVE EXCITABILITY; NERVE FIBER; NERVE POTENTIAL; PRIORITY JOURNAL; SECOND TRIMESTER PREGNANCY; SODIUM CURRENT;

ACTION POTENTIALS; AXONS; CEREBRAL CORTEX; ELECTROPHYSIOLOGY; FEMALE; FETUS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; PREGNANCY; PREGNANCY TRIMESTER, SECOND;

EID: 67651100884     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhn206     Document Type: Article

References (60)

1. Allendoerfer KL, Shatz CJ. 1994. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu Rev Neurosci. 17:185-218.
2. Anderson S, Mione M, Yun K, Rubenstein JL. 1999. Differential origins of neocortical projection and local circuit neurons: role of Dlx genes in neocortical interneuronogenesis. Cereb Cortex. 9:646-654.
3. Ang ES, Jr, Haydar TF, Gluncic V, Rakic P. 2003. Four-dimensional migratory coordinates of GABAergic interneurons in the developing mouse cortex. J Neurosci. 23:5805-5815.
4. Ara C, Massimi M, Devirgiliis Conti L. 2002. Retinoic acid modulates gap junctional intracellular communication in hepatocytes and hepatoma cells. Cell Mol Life Sci. 59:1758-1765.
5. Attwell D, Cohen I, Eisner D, Ohba M, Ojeda C. 1979. The steady state TTX-sensitive (''window'') sodium current in cardiac Purkinje fibres. Pflugers Arch. 379:137-142.
6. Bahrey HL, Moody WJ. 2003. Voltage-gated currents, dye and electrical coupling in the embryonic mouse neocortex. Cereb Cortex. 13:239-251.
7. Barone P, Dehay C, Berland M, Bullier J, Kennedy H. 1995. Developmental remodeling of primate visual cortical pathways. Cereb Cortex. 5:22-38.
8. Bayatti N, Moss JA, Sun L, Ambrose P, Ward JF, Lindsay S, Clowry GJ. 2008. A molecular neuroanatomical study of the developing human neocortex from 8 to 17 postconceptional weeks revealing the early differentiation of the subplate and subventricular zone. Cereb Cortex. 18:1536-1548.
9. Berghs S, Aggujaro D, Dirkx R, Jr., Maksimova E, Stabach P, Hermel JM, Zhang JP, Philbrick W, Slepnev V, Ort T, et al. 2000. BetaIV spectrin, a new spectrin localized at axon initial segments and nodes of ranvier in the central and peripheral nervous system. J Cell Biol. 151:985-1002.
10. Bittman K, Owens DF, Kriegstein AR, Loturco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of developing neocortex. J Neurosci. 17:7037-7044.
11. Bourgeois JP, Goldman-Rakic PS, Rakic P. 1994. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex. 4:78-96.
12. Bourgeois JP, Rakic P. 1993. Changes of synaptic density in the primary visual cortex of the macaque monkey from fetal to adult stage. J Neurosci. 13:2801-2820.
13. Bystron I, Blakemore C, Rakic P. 2008. Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci. 9:110-122.
14. Chan WKI, Takashima S, Feldhaus C, Stoltenburg-Didinger G, Verney C, Yew D, Ulfig N. 2002. Normal and abnormal development of the human cerebral cortex. Neuroembryology. 1:78-90.
15. Colbert CM, Johnston D. 1996. Axonal action-potential initiation and Na+ channel densities in the soma and axon initial segment of subicular pyramidal neurons. J Neurosci. 16:6676-6686.
16. Hanganu IL, Kilb W, Luhmann HJ. 2002. Functional synaptic projections onto subplate neurons in neonatal rat somatosensory cortex. J Neurosci. 22:7165-7176.
17. Hedstrom KL, Xu X, Ogawa Y, Frischknecth R, Seidenbecher CI, Shrager P, Rasband MN. 2007. Neurofascin assembles a specialized extracellular matrix at the axon initial segment. J Cell Biol. 178:875-886.
18. Hille B. 2001. Ion channels of excitable membranes. Sunderland (MA): Sinauer.
19. Howard B, Chen Y, Zecevic N. 2006. Cortical progenitor cells in the developing human telencephalon. Glia. 53:57-66.
20. Huguenard JR, Hamill OP, Prince DA. 1988. Developmental changes in Na+ conductances in rat neocortical neurons: appearance of a slowly inactivating component. J Neurophysiol. 59:778-795.
21. Inda MC, DeFelipe J, Munoz A. 2006. Voltage-gated ion channels in the axon initial segment of human cortical pyramidal cells and their relationship with chandelier cells. Proc Natl Acad Sci USA. 103:2920-2925.
22. Johnson MA, Weick JP, Pearce RA, Zhang SC. 2007. Functional neural development from human embryonic stem cells: accelerated synaptic activity via astrocyte coculture. J Neurosci. 27:3069-3077.
23. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M. 2000. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol. 525(Pt 1):75-81.
24. Kanold PO. 2004. Transient microcircuits formed by subplate neurons and their role in functional development of thalamocortical connections. Neuroreport. 15:2149-2153.
25. Katz LC, Shatz CJ. 1996. Synaptic activity and the construction of cortical circuits. Science. 274:1133-1138.
26. Kerkovich DM, Sapp D, Weidenheim K, Brosnan CF, Pfeiffer SE, Yeh HH, Busciglio J. 1999. Fetal human cortical neurons grown in culture: morphological differentiation, biochemical correlates and development of electrical activity. Int J Dev Neurosci. 17:347-356.
27. Kole MH, Letzkus JJ, Stuart GJ. 2007. Axon initial segment kv1 channels control axonal action potential waveform and synaptic efficacy. Neuron. 55:633-647.
28. Komuro H, Rakic P. 1998. Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. J Neurobiol. 37:110-130.
29. Kornack DR, Rakic P. 1998. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc Natl Acad Sci USA. 95:1242-1246.
30. Korngreen A, Sakmann B. 2000. Voltage-gated K+ channels in layer 5 neocortical pyramidal neurones from young rats: subtypes and gradients. J Physiol. 525(Pt 3):621-639.
31. Kostovic I, Jovanov-Milosevic N. 2006. The development of cerebral connections during the first 20-45 weeks' gestation. Semin Fetal Neonatal Med. 11:415-422.
32. Kostovic I, Rakic P. 1990. Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol. 297:441-470.
33. Kriegstein AR, Gotz M. 2003. Radial glia diversity: a matter of cell fate. Glia. 43:37-43.
34. Kriegstein A, Parnavelas JG. 2003. Changing concepts of cortical development. Cereb Cortex. 13:541.
35. Letinic K, Zoncu R, Rakic P. 2002. Origin of GABAergic neurons in the human neocortex. Nature. 417:645-649.
36. Levitt P. 2003. Structural and functional maturation of the developing primate brain. J Pediatr. 143:S35-45.
37. Levitt P. 2005. Developmental neurobiology and clinical disorders: lost in translation? Neuron. 46:407-412.
38. Luhmann HJ, Reiprich RA, Hanganu I, Kilb W. 2000. Cellular physiology of the neonatal rat cerebral cortex: intrinsic membrane properties, sodium and calcium currents. J Neurosci Res. 62:574-584.
39. Luhmann HJ, Schubert D, Kotter R, Staiger JF. 1999. Cellular morphology and physiology of the perinatal rat cerebral cortex. Dev Neurosci. 21:298-309.
40. Marin O, Rubenstein JL. 2001. A long, remarkable journey: tangential migration in the telencephalon. Nat Rev Neurosci. 2:780-790.
41. Marin-Padilla M. 1992. Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J Comp Neurol. 321:223-240.
42. Maynard TM, Sikich L, Lieberman JA, LaMantia AS. 2001. Neural development, cell-cell signaling, and the ''two-hit'' hypothesis of schizophrenia. Schizophr Bull. 27:457-476.
43. McCormick DA, Prince DA. 1987. Post-natal development of electrophysiological properties of rat cerebral cortical pyramidal neurones. J Physiol. 393:743-762.
44. Mo Z, Moore AR, Filipovic R, Ogawa Y, Kazuhiro I, Antic SD, Zecevic N. 2007. Human cortical neurons originate from radial glia and neuronrestricted progenitors. J Neurosci. 27:4132-4145.
45. Moody WJ. 1998. Control of spontaneous activity during development. J Neurobiol. 37:97-109.
46. Moody WJ, Bosma MM. 2005. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol Rev. 85:883-941.
47. Moore AR, Filipovic R, Mo Z, Rasband MN, Zecebic N, Antic SD. 2007. Electrical excitability of young neurons in the human fetal cerebral cortex. Soc Neurosci Abstract. 563.566/D562.
48. Morest DK, Silver J. 2003. Precursors of neurons, neuroglia, and ependymal cells in the CNS: what are they? Where are they from? How do they get where they are going? Glia. 43:6-18.
49. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR. 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci. 7:136-144.
50. Ogawa Y, Schafer DP, Horresh I, Bar V, Hales K, Yang Y, Susuki K, Peles E, Stankewich MC, Rasband MN. 2006. Spectrins and ankyrinb constitute a specialized paranodal cytoskeleton. J Neurosci. 26:5230-5239.
51. Picken Bahrey HL, Moody WJ. 2003. Early development of voltage-gated ion currents and firing properties in neurons of the mouse cerebral cortex. J Neurophysiol. 89:1761-1773.
52. Rakic P. 1972. Mode of cell migration to the superficial layers of fetal monkey neocortex. J Comp Neurol. 145:61-83.
53. Rakic S, Zecevic N. 2003. Emerging complexity of layer in human cerebral cortex. Cereb Cortex. 13:1072-1083.
54. Rasband MN, Peles E, Trimmer JS, Levinson SR, Lux SE, Shrager P. 1999. Dependence of nodal sodium channel clustering on paranodal axoglial contact in the developing CNS. J Neurosci. 19:7516-7528.
55. Sidman R, Rakic P. 1982. Development of the human central nervous system. In: Haymaker W, Adams RD, Haymaker W, Adams RD, editors. Histology and histopathology of the nervous system. Springfield (IL): Charles C. Thomas. p. 3-145.
56. Sidman RL, Rakic P. 1973. Neuronal migration with special reference to developing human brain: a review. Brain Res. 62:1-35.
57. Smith DO, Rosenheimer JL, Kalil RE. 2008. Delayed rectifier and a-type potassium channels associated with kv 2.1 and kv 4.3 expression in embryonic rat neural progenitor cells. PLoS ONE. 3:e1604.
58. Spitzer NC, Kingston PA, Manning TJ, Conklin MW. 2002. Outside and in: development of neuronal excitability. Curr Opin Neurobiol. 12:315-323.
59. Takahashi T, Nowakowski RS, Caviness VS, Jr. 1995. Early ontogeny of the secondary proliferative population of the embryonic murine cerebral wall. J Neurosci. 15:6058-6068.
60. Zecevic N, Chen Y, Filipovic R. 2005. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J Comp Neurol. 491:109-122.