Ontogeny of kainate-induced gamma oscillations in the rat CA3 hippocampus in vitro

Frontiers in Cellular Neuroscience

Volumn 9, Issue MAY, 2015, Pages

  Tsintsadze, Vera ^a,b   Minlebaev, Marat ^a,b,c   Suchkov, Dimitry ^c   Cunningham, Mark O ^d   Khazipov, Roustem ^a,b,c  

^a Turing Center for Living Systems CENTURI Aix Marseille University   (France)

^b AIX MARSEILLE UNIVERSITY   (France)

^c KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Beta; CA3 region; Gaba receptors; Gamma; Hippocampal; Kainate; NKCC1; Oscillations

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BUMETANIDE; CHLORIDE; COTRANSPORTER; GLUTAMATE RECEPTOR; KAINIC ACID;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL SYNCHRONIZATION; ELECTRIC POTENTIAL; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC SYSTEM; HIPPOCAMPAL CA3 REGION; HISTOLOGY; NERVE CELL; NONHUMAN; ONTOGENY; OSCILLATION; PYRAMIDAL NERVE CELL; RAT; SPECTROMETRY; SYNAPSE;

EID: 84929587510     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00195     Document Type: Article

References (66)

1. Bartos, M., Vida, I., and Jonas, P. (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat. Rev. Neurosci. 8, 45-56. doi: 10.1038/nrn2044
2. Ben-Ari, Y. (2002). Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3, 728-739. doi: 10.1038/nrn920
3. Ben-Ari, Y., Cherubini, E., Corradetti, R., and Gaiarsa, J.-L. (1989). Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303-325. doi: 10.1113/jphysiol.1989.sp017762
4. Ben-Ari, Y., Gaiarsa, J. L., Tyzio, R., and Khazipov, R. (2007). GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev. 87, 1215-1284. doi: 10.1152/physrev.00017.2006
5. Buhl, D. L., and Buzsáki, G. (2005). Developmental emergence of hippocampal fast-field ‘‘ripple’’ oscillations in the behaving rat pups. Neuroscience 134, 1423-1430. doi: 10.1016/j.neuroscience.2005.05.030
6. Buhl, E. H., Tamás, G., and Fisahn, A. (1998). Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J. Physiol. 513(Pt. 1), 117-126. doi: 10.1111/j.1469-7793.1998.117by.x
7. Buzsáki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929. doi: 10.1126/science.1099745
8. Buzsáki, G., and Wang, X. J. (2012). Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203-225. doi: 10.1146/annurev-neuro-062111-150444
9. Chattopadhyaya, B., Di Cristo, G., Higashiyama, H., Knott, G. W., Kuhlman, S. J., Welker, E., et al. (2004). Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J. Neurosci. 24, 9598-9611. doi: 10.1523/jneurosci.1851-04.2004
10. Cossart, R. (2011). The maturation of cortical interneuron diversity: how multiple developmental journeys shape the emergence of proper network function. Curr. Opin. Neurobiol. 1, 160-168. doi: 10.1016/j.conb.2010.10.003
11. Csicsvari, J., Jamieson, B., Wise, K. D., and Buzsáki, G. (2003). Mechanisms of gamma oscillations in the hippocampus of the behaving rat. Neuron 37, 311-322. doi: 10.1016/s0896-6273(02)01169-8
12. Daw, M. I., Ashby, M. C., and Isaac, J. T. (2007). Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat. Neurosci. 10, 453-461. doi: 10.1038/nn1866
13. Doischer, D., Hosp, J. A., Yanagawa, Y., Obata, K., Jonas, P., Vida, I., et al. (2008). Postnatal differentiation of basket cells from slow to fast signaling devices. J. Neurosci. 28, 12956-12968. doi: 10.1523/jneurosci.2890-08.2008
14. Du, J., Zhang, L., Weiser, M., Rudy, B., and McBain, C. J. (1996). Developmental expression and functional characterization of the potassium-channel subunit Kv3.1b in parvalbumin-containing interneurons of the rat hippocampus. J. Neurosci. 16, 506-518.
15. Dupuy, S. T., and Houser, C. R. (1996). Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. J. Neurosci. 16, 6919-6932.
16. Dzhala, V., Khalilov, I., Ben-Ari, Y., and Khazipov, R. (2001). Neuronal mechanisms of the anoxia-induced network oscillations in the rat hippocampus in vitro. J. Physiol. 536, 521-531. doi: 10.1111/j.1469-7793.2001.0521c.xd
17. Dzhala, V. I., Talos, D. M., Sdrulla, D. A., Brumback, A. C., Mathews, G. C., Benke, T. A., et al. (2005). NKCC1 transporter facilitates seizures in the developing brain. Nat. Med. 11, 1205-1213. doi: 10.1038/nm1301
18. Fisahn, A., Contractor, A., Traub, R. D., Buhl, E. H., Heinemann, S. F., and McBain, C. J. (2004). Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J. Neurosci. 24, 9658-9668. doi: 10.1523/jneurosci.2973-04.2004
19. Fisahn, A., Pike, F. G., Buhl, E. H., and Paulsen, O. (1998). Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394, 186-189. doi: 10.1038/28179
20. Freeman, J. A., and Nicholson, C. (1975). Experimental optimization of current source-density technique for anuran cerebellum. J. Neurophysiol. 38, 369-382.
21. Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32, 209-224. doi: 10.1146/annurev.neuro.051508.135603
22. Fries, P., Neuenschwander, S., Engel, A. K., Goebel, R., and Singer, W. (2001). Rapid feature selective neuronal synchronization through correlated latency shifting. Nat. Neurosci. 4, 194-200. doi: 10.1038/84032
23. Goldberg, E. M., Jeong, H. Y., Kruglikov, I., Tremblay, R., Lazarenko, R. M., and Rudy, B. (2011). Rapid developmental maturation of neocortical FS cell intrinsic excitability. Cereb. Cortex 21, 666-682. doi: 10.1093/cercor/bhq138
24. Gray, C. M., and Singer, W. (1989). Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc. Natl. Acad. Sci U S A 86, 1698-1702. doi: 10.1073/pnas.86.5.1698
25. Gulyás, A. I., Szabó, G. G., Ulbert, I., Holderith, N., Monyer, H., Erdélyi, F., et al. (2010). Parvalbumin-containing fast-spiking basket cells generate the field potential oscillations induced by cholinergic receptor activation in the hippocampus. J. Neurosci. 30, 15134-15145. doi: 10.1523/jneurosci.4104-10. 2010
26. Haggerty, D. C., Glykos, V., Adams, N. E., and LeBeau, F. E. (2013). Bidirectional modulation of hippocampal gamma(20-80 Hz) frequency activity in vitro via alpha(alpha)- and beta(beta)-adrenergic receptors (AR). Neuroscience 253, 142-154. doi: 10.1016/j.neuroscience.2013.08.028
27. Hájos, N., Katona, I., Naiem, S. S., Mackie, K., Ledent, C., Mody, I., et al. (2000). Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur. J. Neurosci. 12, 3239-3249. doi: 10.1046/j.1460-9568.2000.00217.x
28. Hormuzdi, S. G., Pais, I., LeBeau, F. E., Towers, S. K., Rozov, A., Buhl, E. H., et al. (2001). Impaired electrical signaling disrupts gamma frequency oscillations in connexin 36-deficient mice. Neuron 31, 487-495. doi: 10.1016/s0896-6273(01)00387-7
29. Huang, Z. J., Di Cristo, G., and Ango, F. (2007). Development of GABA innervation in the cerebral and cerebellar cortices. Nat. Rev. Neurosci. 8, 673-686. doi: 10.1038/nrn2188
30. Khalilov, I., Dzhala, V., Medina, I., Leinekugel, X., Melyan, Z., Lamsa, K., et al. (1999). Maturation of kainate-induced epileptiform activities in interconnected intact neonatal limbic structures in vitro. Eur. J. Neurosci. 11, 3468-3480. doi: 10.1046/j.1460-9568.1999.00768.x
31. Khazipov, R., and Holmes, G. L. (2003). Synchronization of kainate-induced epileptic activity via GABAergic inhibition in the superfused rat hippocampus in vivo. J. Neurosci. 23, 5337-5341.
32. Khazipov, R., Khalilov, I., Tyzio, R., Morozova, E., Ben Ari, Y., and Holmes, G. L. (2004). Developmental changes in GABAergic actions and seizure susceptibility in the rat hippocampus. Eur. J. Neurosci. 19, 590-600. doi: 10.1111/j.0953-816x.2003.03152.x
33. Khazipov, R., Leinekugel, X., Khalilov, I., Gaïarsa, J.-L., and Ben-Ari, Y. (1997). Synchronization of GABAergic interneuronal network in CA3 subfield of neonatal rat hippocampal slices. J. Physiol. 498, 763-772. doi: 10.1113/jphysiol.1997.sp021900
34. Khazipov, R., Minlebaev, M., and Valeeva, G. (2013). Early gamma oscillations. Neuroscience 250, 240-252. doi: 10.1016/j.neuroscience.2013.07.019
35. Khazipov, R., Valeeva, G., and Khalilov, I. (2015). Depolarizing GABA and developmental epilepsies. CNS Neurosci. Ther. 21, 83-91. doi: 10.1111/cns.12353
36. Khirug, S., Ahmad, F., Puskarjov, M., Afzalov, R., Kaila, K., and Blaesse, P. (2010). A single seizure episode leads to rapid functional activation of KCC2 in the neonatal rat hippocampus. J. Neurosci. 30, 12028-12035. doi: 10.1523/jneurosci.3154-10.2010
37. Lahtinen, H., Palva, J. M., Sumanen, S., Voipio, J., Kaila, K., and Taira, T. (2002). Postnatal development of rat hippocampal gamma rhythm in vivo. J. Neurophysiol. 88, 1469-1474. doi: 10.1152/jn.00800.2001
38. Le, M. C., and Monyer, H. (2013). GABAergic interneurons shape the functional maturation of the cortex. Neuron 77, 388-405. doi: 10.1016/j.neuron.2013.01.011
39. Leinekugel, X., Khazipov, R., Cannon, R., Hirase, H., Ben Ari, Y., and Buzsáki, G. (2002). Correlated bursts of activity in the neonatal hippocampus in vivo. Science 296, 2049-2052. doi: 10.1126/science.1071111
40. Mann, E. O., and Paulsen, O. (2007). Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 30, 343-349. doi: 10.1016/j.tins.2007.05.003
41. Mann, E. O., Suckling, J. M., Hajos, N., Greenfield, S. A., and Paulsen, O. (2005). Perisomatic feedback inhibition underlies cholinergically induced fast network oscillations in the rat hippocampus in vitro. Neuron 45, 105-117. doi: 10.1016/j.neuron.2004.12.016
42. Minlebaev, M., Colonnese, M., Tsintsadze, T., Sirota, A., and Khazipov, R. (2011). Early gamma oscillations synchronize developing thalamus and cortex. Science 334, 226-229. doi: 10.1126/science.1210574
43. Minlebaev, M., Valeeva, G., Tcheremiskine, V., Coustillier, G., and Khazipov, R. (2013). Cell-attached recordings of responses evoked by photorelease of GABA in the immature cortical neurons. Front. Cell. Neurosci. 7:83. doi: 10.3389/fncel.2013.00083
44. Mitra, P. P., and Pesaran, B. (1999). Analysis of dynamic brain imaging data. Biophys. J. 76, 691-708. doi: 10.1016/s0006-3495(99)77236-x
45. Mohns, E. J., and Blumberg, M. S. (2008). Synchronous bursts of neuronal activity in the developing hippocampus: modulation by active sleep and association with emerging gamma and theta rhythms. J. Neurosci. 28, 10134-10144. doi: 10.1523/jneurosci.1967-08.2008
46. Okaty, B. W., Miller, M. N., Sugino, K., Hempel, C. M., and Nelson, S. B. (2009). Transcriptional and electrophysiological maturation of neocortical fast-spiking GABAergic interneurons. J. Neurosci. 29, 7040-7052. doi: 10.1523/jneurosci.0105-09.2009
47. Oren, I., Hájos, N., and Paulsen, O. (2010). Identification of the current generator underlying cholinergically induced gamma frequency field potential oscillations in the hippocampal CA3 region. J. Physiol. 588, 785-797. doi: 10.1113/jphysiol.2009.180851
48. Pais, I., Hormuzdi, S. G., Monyer, H., Traub, R. D., Wood, I. C., Buhl, E. H., et al. (2003). Sharp wave-like activity in the hippocampus in vitro in mice lacking the gap junction protein connexin 36. J. Neurophysiol. 89, 2046-2054. doi: 10.1152/jn.00549.2002
49. Pangratz-Fuehrer, S., and 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
50. Sakatani, S., Seto-Ohshima, A., Shinohara, Y., Yamamoto, Y., Yamamoto, H., Itohara, S., et al. (2008). Neural-activity-dependent release of S100B from astrocytes enhances kainate-induced gamma oscillations in vivo. J. Neurosci. 28, 10928-10936. doi: 10.1523/jneurosci.3693-08.2008
51. Sauer, J. F., and Bartos, M. (2010). Recruitment of early postnatal parvalbumin- positive hippocampal interneurons by GABAergic excitation. J. Neurosci. 30, 110-115. doi: 10.1523/JNEUROSCI.4125-09.2010
52. Singer, W., and Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586. doi: 10.1146/annurev.neuro.18.1.555
53. Sipilä, S. T., Schuchmann, S., Voipio, J., Yamada, J., and Kaila, K. (2006). The cation-chloride cotransporter NKCC1 promotes sharp waves in the neonatal rat hippocampus. J. Physiol. 573, 765-773. doi: 10.1113/jphysiol.2006.107086
54. Taketo, M., and Yoshioka, T. (2000). Developmental change of GABA(A) receptor-mediated current in rat hippocampus. Neuroscience 96, 507-514. doi: 10.1016/s0306-4522(99)00574-6
55. Traub, R. D., Jefferys, J. G., and Whittington, M. A. (1997). Simulation of gamma rhythms in networks of interneurons and pyramidalX cells. J. Comput. Neurosci. 4, 141-150. doi: 10.1023/A:1008839312043
56. Tyzio, R., Cossart, R., Khalilov, I., Minlebaev, M., Hübner, C. A., Represa, A., et al. (2006). Maternal oxytocin triggers a transient inhibitory switch in GABA signaling in the fetal brain during delivery. Science 314, 1788-1792. doi: 10.1126/science.1133212
57. Tyzio, R., Minlebaev, M., Rheims, S., Ivanov, A., Jorquera, I., Holmes, G. L., et al. (2008). Postnatal changes in somatic gamma-aminobutyric acid signalling in the rat hippocampus. Eur. J. Neurosci. 27, 2515-2528. doi: 10.1111/j.1460-9568.2008.06234.x
58. Tyzio, R., Represa, A., Jorquera, I., Ben-Ari, Y., Gozlan, H., and Aniksztejn, L. (1999). The establishment of GABAergic and glutamatergic synapses on CA1 pyramidal neurons is sequential and correlates with the development of the apical dendrite. J. Neurosci. 19, 10372-10382.
59. Uhlhaas, P. J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A., and Singer, W. (2010). Neural synchrony and the development of cortical networks. Trends Cogn. Sci. 14, 72-80. doi: 10.1016/j.tics.2009.12.002
60. Valeeva, G., Abdullin, A., Tyzio, R., Skorinkin, A., Nikolski, E., Ben-Ari, Y., et al. (2010). Temporal coding at the immature depolarizing GABAergic synapse. Front. Cell. Neurosci. 4:17. doi: 10.3389/fncel.2010.00017
61. Valeeva, G., Valiullina, F., and Khazipov, R. (2013). Excitatory actions of GABA in the intact neonatal rodent hippocampus in vitro. Front. Cell. Neurosci. 7:20. doi: 10.3389/fncel.2013.00020
62. Wang, X. J. (2010). Neurophysiological and computational principles of cortical rhythms in cognition. Physiol. Rev. 90, 1195-1268. doi: 10.1152/physrev.00035.2008
63. Wang, H. X., and Gao, W. J. (2010). Development of calcium-permeable AMPA receptors and their correlation with NMDA receptors in fast-spiking interneurons of rat prefrontal cortex. J. Physiol. 588, 2823-2838. doi: 10.1113/jphysiol.2010.187591
64. Whittington, M. A., Cunningham, M. O., LeBeau, F. E., Racca, C., and Traub, R. D. (2011). Multiple origins of the cortical gamma rhythm. Dev. Neurobiol. 71, 92-106. doi: 10.1002/dneu.20814
65. Yamada, J., Okabe, A., Toyoda, H., Kilb, W., Luhmann, H. J., and Fukuda, A. (2004). Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J. Physiol. 557, 829-841. doi: 10.1113/jphysiol.2004.062471
66. Yang, J. M., Zhang, J., Yu, Y. Q., Duan, S., and Li, X. M. (2014). Postnatal development of 2 microcircuits involving fast-spiking interneurons in the mouse prefrontal cortex. Cereb. Cortex 1, 98-109. doi: 10.1093/cercor/bhs291