Interneurons and oligodendrocyte progenitors form a structured synaptic network in the developing neocortex

eLife

Volumn 2015, Issue 4, 2015, Pages 1-53

  Orduz, David ^a,b   Maldonado, Paloma P ^a,b,e   Balia, Maddalena ^a,b   Vélez Fort, Mateo ^a,b,f   de Sars, Vincent ^b,c   Yanagawa, Yuchio ^d   Emiliani, Valentina ^b,c   Angulo, María Cecilia ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c CNRS   (France)

^d GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^f NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; BENZODIAZEPINE; CYTOCHROME C1; DIAZEPAM; GLUTAMATE SODIUM; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; BACTERIAL PROTEIN; FLUORESCENT PROTEIN 583; PHOTOPROTEIN; PROTEIN SUBUNIT; YELLOW FLUORESCENT PROTEIN, BACTERIA;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CONNECTOME; EXCITATORY POSTSYNAPTIC POTENTIAL; INTERNEURON; NEOCORTEX; NEUROMUSCULAR SYNAPSE; NONHUMAN; OLIGODENDROCYTE PRECURSOR CELL; PATCH CLAMP TECHNIQUE; PHOTOLYSIS; TRANSGENIC MOUSE; ACTION POTENTIAL; ANIMAL; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROTOMY; MOUSE; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; OLIGODENDROGLIA; PHYSIOLOGY; PROTEIN SUBUNIT; REPORTER GENE; SOMATOSENSORY CORTEX; SYNAPSE; SYNAPTIC TRANSMISSION; TISSUE CULTURE TECHNIQUE; ULTRASTRUCTURE;

ACTION POTENTIALS; ANIMALS; BACTERIAL PROTEINS; CELL DIFFERENTIATION; GAMMA-AMINOBUTYRIC ACID; GENE EXPRESSION; GENES, REPORTER; INTERNEURONS; LUMINESCENT PROTEINS; MICE; MICE, TRANSGENIC; MICROTOMY; NEOCORTEX; NEURAL STEM CELLS; NEUROGENESIS; OLIGODENDROGLIA; PATCH-CLAMP TECHNIQUES; PROTEIN SUBUNITS; RECEPTORS, GABA-A; SOMATOSENSORY CORTEX; SYNAPSES; SYNAPTIC TRANSMISSION; TISSUE CULTURE TECHNIQUES;

EID: 84929167721     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Ali AB, Thomson AM. 2008. Synaptic alpha 5 subunit-containing GABAA receptors mediate IPSPs elicited by dendrite-preferring cells in rat neocortex. Cereb Cortex 18:1260-1271. doi: 10.1093/cercor/bhm160.
2. Angulo MC, Staiger JF, Rossier J, Audinat E. 1999. Developmental synaptic changes increase the range of integrative capabilities of an identified excitatory neocortical connection. J Neurosci 19:1566-1576.
3. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R. 2008. Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557-568. doi: 10.1038/nrn2402.
4. Balia M, Velez-Fort M, Passlick S, Schafer C, Audinat E, Steinhauser C, Seifert G, Angulo MC. 2015. Postnatal Down-Regulation of the GABAA Receptor gamma2 Subunit in Neocortical NG2 Cells Accompanies Synaptic-to-Extrasynaptic Switch in the GABAergic Transmission Mode. Cereb Cortex. 25:1114-1123. doi: 10.1093/cercor/bht309.
5. Baracskay KL, Duchala CS, Miller RH, Macklin WB, Trapp BD. 2002. Oligodendrogenesis is differentially regulated in gray and white matter of jimpy mice. J Neurosci Res 70:645-654.
6. Barres BA, Hart IK, Coles HS, Burne JF, Voyvodic JT, Richardson WD, Raff MC. 1992. Cell death and control of cell survival in the oligodendrocyte lineage. Cell 70:31-46.
7. Bergles DE, Roberts JD, Somogyi P, Jahr CE. 2000. Glutamatergic synapses on oligodendrocyte precursor cells in the hippocampus. Nature 405:187-191.
8. Cauli B, Audinat E, Lambolez B, Angulo MC, Ropert N, Tsuzuki K, Hestrin S, Rossier J. 1997. Molecular and physiological diversity of cortical nonpyramidal cells. J Neurosci 17:3894-3906.
9. Cossart R. 2011. The maturation of cortical interneuron diversity: how multiple developmental journeys shape the emergence of proper network function. Curr Opin Neurobiol 21:160-168. doi:10.1016/j.conb.2010.10.003.
10. Dantzker JL, Callaway EM. 2000. Laminar sources of synaptic input to cortical inhibitory interneurons and pyramidal neurons. Nat Neurosci 3:701-707. doi: 10.1038/76656.
11. Daw MI, Ashby MC, Isaac JT. 2007. Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat Neurosci 10:453-461. doi: 10.1038/nn1866.
12. De Biase LM, Nishiyama A, Bergles DE. 2010. Excitability and synaptic communication within the oligodendrocyte lineage. J Neurosci 30:3600-3611. doi: 10.1523/JNEUROSCI.6000-09.2010.
13. Fino E, Araya R, Peterka DS, Salierno M, Etchenique R, Yuste R. 2009. RuBi-Glutamate: Two-Photon and Visible-Light Photoactivation of Neurons and Dendritic spines. Front Neural Circuits 3:2. doi: 10.3389/neuro.04.002.2009.
14. Fino E, Yuste R. 2011. Dense inhibitory connectivity in neocortex. Neuron 69:1188-1203. doi: 10.1016/j.neuron.2011.02.025.
15. Fishell G, Rudy B. 2011. Mechanisms of inhibition within the telencephalon: "where the wild things are". Annu Rev Neurosci 34:535-567. doi: 10.1146/annurev-neuro-061010-113717.
16. Golomb D, Donner K, Shacham L, Shlosberg D, Amitai Y, Hansel D. 2007. Mechanisms of firing patterns in fast-spiking cortical interneurons. PLoS Comput Biol 3:e156. doi: 10.1371/journal.pcbi.0030156.
17. Huang ZJ, Di Cristo G, Ango F. 2007. Development of GABA innervation in the cerebral and cerebellar cortices. Nat Rev Neurosci 8:673-686. doi: 10.1038/nrn2188.
18. Kessaris N, Fogarty M, Iannarelli P, Grist M, Wegner M, Richardson WD. 2006. Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat Neurosci 9:173-179. doi: 10.1038/nn1620.
19. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321:53-57. doi: 10.1126/science.1149381.
20. Kressin K, Kuprijanova E, Jabs R, Seifert G, Steinhauser C. 1995. Developmental regulation of Na+ and K+ conductances in glial cells of mouse hippocampal brain slices. Glia 15:173-187. doi: 10.1002/glia.440150210.
21. Kukley M, Nishiyama A, Dietrich D. 2010. The fate of synaptic input to NG2 glial cells: neurons specifically downregulate transmitter release onto differentiating oligodendroglial cells. J Neurosci 30:8320-8331. doi: 10.1523/JNEUROSCL0854-10.2010.
22. Lawrence D, Brown T, Cai T, DasGupta A. 2001. Interval Estimation for a Binomial Proportion. Statistical Science 16:101-133.
23. Lutz C, Otis TS, Desars V, Charpak S, Digregorio DA, Emiliani V. 2008. Holographic photolysis of caged neurotransmitters. Nat Methods. 5(9):821-7. doi: 10.1038/nmeth.1241.
24. Maldonado PP, Angulo MC. 2014. Multiple Modes of Communication between Neurons and Oligodendrocyte Precursor Cells. Neuroscientist doi: 10.1177/1073858414530784.
25. Maldonado PP, Velez-Fort M, Levavasseur F, Angulo MC. 2013. Oligodendrocyte precursor cells are accurate sensors of local K+ in mature gray matter. J Neurosci 33:2432-2442. doi: 10.1523/JNEUROSCI.1961-12.2013.
26. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. 2001. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086-1092. doi: 10.1038/nn736.
27. Okaty BW, Miller MN, Sugino K, Hempel CM, Nelson SB. 2009. Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. J Neurosci 29:7040-7052. doi: 10.1523/JNEUROSCI.0105-09.2009.
28. Packer AM, McConnell DJ, Fino E, Yuste R. 2014. Axo-dendritic overlap and laminar projection can explain interneuron connectivity to pyramidal cells. Cereb Cortex 23:2790-2802. doi: 10.1093/cercor/bhs210.
29. Pangratz-Fuehrer S, Hestrin S. 2011. Synaptogenesis of electrical and GABAergic synapses of fast- spiking inhibitory neurons in the neocortex. J Neurosci 31:10767-10775. doi: 10.1523/JNEUROSCI.6655-10.2011.
30. Passlick S, Grauer M, Schafer C, Jabs R, Seifert G, Steinhauser C. 2013. Expression of the gamma2- subunit distinguishes synaptic and extrasynaptic GABA(A) receptors in NG2 cells of the hippocampus. J Neurosci 33:12030-12040. doi: 10.1523/JNEUROSCI.5562-12.2013.
31. Pearce RA. 1993. Physiological evidence for two distinct GABAA responses in rat hippocampus. Neuron 10:189-200.
32. Pfeffer CK, Xue M, He M, Huang ZJ, Scanziani M. 2013. Inhibition of inhibition in visual cortex: the logic of connections between molecularly distinct interneurons. Nat Neurosci 16:1068-1076. doi: 10.1038/nn.3446.
33. Rasband MN, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, Shrager P. 1998. Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 18:36-47.
34. Shepherd GM, Pologruto TA, Svoboda K. 2003. Circuit analysis of experience-dependent plasticity in the developing rat barrel cortex. Neuron 38:277-289.
35. Somogyi P, Kisvarday ZF, Martin KA, Whitteridge D. 1983. Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261-294.
36. Stevens CF, Wang Y 1995. Facilitation and depression at single central synapses. Neuron 14:795-802.
37. Tong XP, Li XY, Zhou B, Shen W, Zhang ZJ, Xu TL, Duan S. 2009. Ca(2+) signaling evoked by activation of Na(+) channels and Na(+)/Ca(2+) exchangers is required for GABA-induced NG2 cell migration. J Cell Biol 186:113-128.
38. Trapp BD, Nishiyama A, Cheng D, Macklin W. 1997. Differentiation and death of premyelinating oligodendrocytes in developing rodent brain. J Cell Biol 137:459-468.
39. Velez-Fort M, Maldonado PP, Butt AM, Audinat E, Angulo MC. 2010. Postnatal switch from synaptic to extrasynaptic transmission between interneurons and NG2 cells. J Neurosci 30:6921-6929.
40. Wang Y, Kakizaki T, Sakagami H, Saito K, Ebihara S, Kato M, Hirabayashi M, Saito Y, Furuya N, Yanagawa Y 2009. Fluorescent labeling of both GABAergic and glycinergic neurons in vesicular GABA transporter (VGAT)-venus transgenic mouse. Neuroscience 164:1031-1043. doi: 10.1016/j.neuroscience.2009.09.010.
41. 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 24:98-109. doi: 10.1093/cercor/bhs291.
42. Yoshimura Y, Dantzker JL, Callaway EM. 2005. Excitatory cortical neurons form fine-scale functional networks. Nature 433:868-873. doi: 10.1038/nature03252.
43. Zahid M, Velez-Fort M, Papagiakoumou E, Ventalon C, Angulo MC, Emiliani V 2010. Holographic photolysis for multiple cell stimulation in mouse hippocampal slices. PLoS One 5:e9431.
44. Zalc B, Fields RD. 2000. Do Action Potentials Regulate Myelination? Neuroscientist 6:5-13.
45. Ziskin JL, Nishiyama A, Rubio M, Fukaya M, Bergles DE. 2007. Vesicular release of glutamate from unmyelinated axons in white matter. Nat Neurosci 10:321-330.