In vivo calcium imaging of evoked calcium waves in the embryonic cortex

Frontiers in Cellular Neuroscience

Volumn 9, Issue JAN2016, 2016, Pages

  Yuryev, Mikhail ^a   Pellegrino, Christophe ^b,c   Jokinen, Ville ^d   Andriichuk, Liliia ^a   Khirug, Stanislav ^a   Khiroug, Leonard ^a   Riverat, Claudio ^a,b,c  

^a UNIVERSITY OF HELSINKI   (Finland)

^b INSERM   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d AALTO UNIVERSITY   (Finland)

Author keywords

Calcium imaging; Cortical development; In vivo imaging; Purinergic receptors; Two photon microscopy

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM; PURINERGIC RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUTISM; BRAIN CORTEX; BRAIN DEVELOPMENT; CALCIUM SIGNALING; CALCIUM TRANSPORT; EMBRYONIC STRUCTURES; FEMALE; IMAGE PROCESSING; IMMOBILIZATION; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; PHOTOSTIMULATION; SCHIZOPHRENIA; SIGNAL TRANSDUCTION;

EID: 84957831085     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00500     Document Type: Article

References (41)

1. Allène, C., Cattani, A., Ackman, J. B., Bonifazi, P., Aniksztejn, L., Ben-Ari, Y., et al. (2008). Sequential generation of two distinct synapse-driven network patterns in developing neocortex. J. Neurosci. 28, 12851-12863. doi: 10.1523/JNEUR0SCI.3733-08.2008
2. Allène, C., and Cossart, R. (2010). Early NMDA receptor-driven waves of activity in the developing neocortex: physiological or pathological network oscillations? J. Physiol. 588, 83-91. doi: 10.1113/jphysiol.2009.178798
3. Brustein, E., Marandi, N., Kovalchuk, Y., Drapeau, P., and Konnerh, A. (2003). “In vivo" monitoring of neuronal network activity in zebrafish by two-photon Ca2+ imaging. PflugersArch. 446,766-773. doi: 10.1007/s00424-003-1138-4
4. Caetano, S. S., Teixeira, T., and Tadokoro, C. E. (2012). Intravital imaging of the mouse thymus using 2-photon microscopy. J. Vis. Exp. 59:e3504. doi: 10.3791/3504
5. Caviness, V. S. Jr., Takahashi, T., and Nowakowski, R. S. (1995). Numbers, time and neocortical neuronogenesis: a general developmental and evolutionary model. TrendsNeurosci. 18, 379-383.doi: 10.1016/0166-2236(95)93933-0
6. Chang, L. W., and Spitzer, N. C. (2009). Spontaneous calcium spike activity in embryonic spinal neurons is regulated by developmental expression of the Na+, K+-ATPase β3 subunit. J. Neurosci. 29, 7877-7885. doi: 10.1523/JNEUR0SCI.4264-08.2009
7. Conhaim, J., Cedarbaum, E. R., Barahimi, M., Moore, J. G., Becker, M. I., Gleiss, H., et al. (2010). Bimodal septal and cortical triggering and complex propagation patterns of spontaneous waves of activity in the developing mouse cerebral cortex. Dev. Neurobiol. 70, 679-692. doi: 10.1002/dneu.20797
8. Corlew, R., Bosma, M. M., and Moody, W. J. (2004). Spontaneous, synchronous electrical activity in neonatal mouse cortical neurones. J. Physiol. 560, 377-390. doi: 10.1113/jphysiol.2004.071621
9. Crepel, V., Aronov, D., Jorquera, I., Represa, A., Ben-Ari, Y., and Cossart, R. (2007). A parturition-associated nonsynaptic coherent activity pattern in the developing hippocampus. Neuron 54, 105-120. doi: 10.1016/j.neuron.2007.03.007
10. D'Amour, K. A., and Gage, F. H. (2003). Genetic and functional differences between multipotent neural and pluripotent embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 100(Suppl 1), 11866-11872. doi: 10.1073/pnas.1834200100
11. Fligny, C., Hatia, S., Amireault, P., Mallet, J., and Cote, F. (2009). Mammalian prenatal development: the influence of maternally derived molecules. Bioessays 31, 935-943. doi: 10.1002/bies.200800217
12. Friel, D. D., and Tsien, R. W. (1992). A caffeine-and ryanodine-sensitive Ca2+ store in bullfrog sympathetic neurones modulates effects of Ca2+ entry on [Ca2+]i. J. Physiol. 450,217-246. doi: 10.1113/jphysiol.1992.sp019125
13. Garaschuk, O., Linn, J., Eilers, J., and Konnerth, A. (2000). Large-scale oscillatory calcium waves in the immature cortex. Nat. Neurosci. 4, 452-459. doi: 10.1038/74823
14. Gust, J., Wright, J. J., Pratt, E. B., and Bosma, M. M. (2003). Development of synchronized activity of cranial motor neurons in the segmented embryonic mouse hindbrain. J. Physiol. 550, 123-133. doi: 10.1113/jphysiol.2002.038737
15. Guthrie, P. B., Knappenberger, J., Segal, M., Bennett, M. V., Charles, A. C., and Kater, S. B. (1999). ATP released from astrocytes mediates glial calcium waves. J. Neurosci. 19, 520-528.
16. Huang, X., Troy, W. C., Yang, Q., Ma, H., Laing, C. R., Schiff, S. J., et al. (2004). Spiral waves in disinhibited mammalian neocortex. J. Neurosci. 22, 9897-9902. doi: 10.1523/JNEUR0SCI.2705-04.2004
17. Hunt, P. N., McCabe, A. K., and Bosma, M. M. (2005). Midline serotonergic neurones contribute to widespread synchronized activity in embryonic mouse hindbrain. J. Physiol. 566, 807-819. doi: 10.1113/jphysiol.2005.089581
18. Komuro, H., and Rakic, P. (1993). Modulation of neuronal migration by NMDA receptors. Science 260, 95-97. doi: 10.1126/science.8096653
19. Komuro, H., and Rakic, P. (1996). Intracellular Ca2+ fluctuations modulate the rate of neuronal migration. Neuron 17, 275-285. doi: 10.1016/S0896-6273(00)80159-2
20. Kriegstein, A. R., and Noctor, S. C. (2004). Patterns of neuronal migration in the embryonic cortex. Trends Neurosci. 27, 392-399. doi: 10.1016/j.tins.2004.05.001
21. Kwan, K. Y., Sestan, N., and Anton, E. S. (2012). Transcriptional co-regulation of neuronal migration and laminar identity in the neocortex. Development 139, 1535-1546. doi: 10.1242/dev.069963
22. Leinekugel, X., Khalilov, I., Ben-Ari, Y., and Khazipov, R. (1998). Giant depolarizing potentials: the septal pole of the hippocampus paces the activity of the developing intact septohippocampal complex in vitro. J. Neurosci. 18, 6349-6357.
23. Lischalk, J. W., Easton, C. R., and Moody, W. J. (2009). Bilaterally propagating waves of spontaneous activity arising from discrete pacemakers in the neonatal mouse cerebral cortex. Dev. Neurobiol. 69, 407-414. doi: 10.1002/dneu.20708
24. Liu, X., Hashimoto-Torii, K., Torii, M., Ding, C., and Rakic, P. (2010). Gap junctions/hemichannels modulate interkinetic nuclear migration in the forebrain precursors. J. Neurosci. 30, 4197-4209. doi: 10.1523/JNEUR0SCI.4187-09.2010
25. McKinney, M. C., and Kulesa, P. M. (2011). In vivo calcium dynamics during neural crest cell migration and patterning using GCaMP3. Dev. Biol. 358, 309-317. doi: 10.1016/j.ydbio.2011.08.004
26. Meister, M., Wong, R. O., Baylor, D. A., and Shatz, C. J. (1991). Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939-943. doi: 10.1126/science.2035024
27. Moisiadis, V. G., and Matthews, S. G. (2014). Glucocorticoids and fetal programming part 2: Mechanisms. Nat. Rev. Endocrinol. 10, 403-411. doi: 10.1038/nrendo.2014.74
28. Montoro, R. J., and Yuste, R. (2004). Gap junctions in developing neocortex: a review. Brain Res. Rev. 47, 216-226. doi: 10.1016/j.brainresrev.2004.06.009
29. Nunes, A. R., Chavez-Valdez, R., Ezell, T., Donnelly, D. F., Glover, J. C., and Gauda, E. B. (2012). Effect of development on [Ca2+]i transients to ATP in petrosal ganglion neurons: a pharmacological approach using optical recording. J. Appl. Physiol. 112, 1393-1402.doi: 10.1152/japplphysiol.00511.2011
30. O'Donovan, M. J., Chub, N., and Wenner, P. (1998). Mechanisms of spontaneous activity in developing spinal networks. J. Neurobiol. 37, 131-145.
31. Owens, D. F., and Kriegstein, A. R. (1998). Patterns of intracellular calcium fluctuation in precursor cells ofthe neocortical ventricular zone. J. Neurosci. 18, 5374-5388.
32. Pierfelice, T. J., and Gaiano, N. (2010). Ultrasound-guided microinjection into the mouse forebrain in utero at E9.5. J. Vis. Exp. 45:e2047. doi: 10.3791/2047
33. Preibisch, S., Saalfeld, S., Schindelin, J., and Tomancak, P. (2010). Software for bead-based registration of selective plane illumination microscopy data. Nat. Methods 7,418-419. doi: 10.1038/nmeth0610-418
34. Rockhill, W., Kirkman, J. L., and Bosma, M. M. (2009). Spontaneous activity in the developing mouse midbrain driven by an external pacemaker. Dev. Neurobiol. 69, 689-704. doi: 10.1002/dneu.20725
35. Ross, W. N. (2012). Understanding calcium waves and sparks in central neurons. Nat. Rev. Neurosci. 13, 157-168. doi: 10.1038/nrn3168
36. Smith, N. I., Fujita, K., Kaneko, T., Katoh, K., Nakamura, O., Kawata, S., et al. (2001). Generation of calcium waves in living cells by pulsed-laser-induced photodisruption. Appl. Phys. Lett. 79, 1208-1210. doi: 10.1063/1.1397255
37. Sorzano, C. O., Thevenaz, P., and Unser, M. (2005). Elastic registration of biological images using vector-spline regularization. IEEE Trans. Biomed. Eng. 52, 652-663. doi: 10.1109/TBME.2005.844030
38. Spitzer, N. C. (2006). Electrical activityin earlyneuronal development. Nature 444, 707-712. doi: 10.1038/nature05300
39. Thevenaz, P., Ruttimann, U. E., and Unser, M. A. (1998). A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27-41. doi: 10.1109/83.650848
40. Tremblay, M., Fugere, V., Tsui, J., Schohl, A., Tavakoli, A., Travenôlo, B. A., et al. (2009). Regulation of radial glial motility by visual experience. J. Neurosci. 29, 14066-14076. doi: 10.1523/JNEUROSCI.3542-09.2009
41. Weissman, T. A., Riquelme, P. A., Ivic, L., Flint, A. C., and Kriegstein, A. R. (2004). Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43, 647-661. doi: 10.1016/j.neuron.2004.08.015