Abstract
Complex but coordinated interactions involving ensembles of neuronal cells result in the accurate processing of information in the adult central nervous system. However, recent studies monitoring the global patterns of activity of neuronal populations have demonstrated that immature neurons also interact to produce coordinated patterns of activity during the early stages of development. In particular, these patterns of coordinated activity occur during the period when neuronal connections are established, thus leading us to believe that such activity patterns might underlie the precision to which many neural pathways are wired up. Multielectrode recording and calcium imaging are two of the techniques that have been intstrumental in revealing the spatial and temporal properties of the coordinated activity of developing neural networks in vitro. While multielectrode arrays measure the action potential activity of the cells, calcium imaging permits changes in intracellular calcium levels to be monitored over time. Both techniques have been used successfully to monitor the activity of cellular networks in culture, but they have also been applied in assessing the patterns of activity in intact or semi-intact pieces of neural tissues, such as the developing retina, neocortex and spinal cord. More recently, it has also been possible to correlate the structure and function of the cellular components of the networks by combining intracellular dye filling with the multineuronal recordings. In this review, brief descriptions and the applications of the two techniques will be presented, and the advantages and limitations of multielectrode array will be compared with that of calcium imaging using recordings of the developing mammalian retina as the primary example. 1998 © Chapman & Hall
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baldridge, W. (1996) Optical recordings of the effects of cholinergic ligands on neurons in the ganglion cell layer of mammalian retina. J. Neurosci. 16, 5060–72.
Bonhoeffer, T. (1995) Optical imaging of intrinsic signals as a tool to visualize the functional architecture of adult and developing visual cortex. Arzneimittel-Forschung 45, 351–6.
Callaway, E.M. & Katz, L.C. (1993) Photostimulation using caged glutamate reveals funtional circuitry in living brain slices. Proc. Natl. Acad. Sci. USA 90, 7661–5.
Dailey, M.E. & Smith, S.J. (1994) Spontaneous Ca2+ transients in developing hippocampal pyramidal cells. J. Neurobiol. 25, 243–51.
Droge, M.H., Gross, G.W., Hightower, M.H. & Czisny, L.E. (1986) Multielectrode analysis of coordinated, rhythmic bursting in cultured CNS monolayer networks. J. Neurosci. 6, 1583–92.
Feller, M.B., Wellis, D.P., Stellwagen, D., Werblin, F.S. & Shatz, C. J. (1996) Requirement for cholinergic transmission in the propagation of spontaneous retinal waves. Science 272, 1182–6.
Godecke, I. & Bonhoeffer, T. (1996) Development of identical orientation maps for two eyes without common visual experience. Nature 379, 251–4.
Goodman, C.S. & Shatz, C. J. (1993) Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell 72/ Neuron 10 (Suppl.), 77–98.
Gross, G.W. (1979) Simultaneous single unit recording in vitro with a photoetched, laser deinsulated gold multimicroelectrode surface. IEEE Trans. Biomed. Eng. 26, 273–9.
Gross, G.W. & Lucas, J.H. (1982) Long-term monitoring of spontaneous single unit activity from neuronal monolayer networks cultured on photoetched multielectrode surface. J. Electrophys. Tech. 9, 55–69.
Gross, G.W., Wen, W.Y. & Lin, J.W. (1985) Transparent indium-tin electrode patterns for extracellular, multisite recording in neuronal cultures. J. Neurosci. Methods 15, 243–52.
Haugland, R (1993) Intracellular ion indicators. In Fluorescent and Luminescent Probes for Biological Activity (edited by Mason, W.T.), pp. 34–43. London: Academic Press.
Jimbo, Y., Robinson, H.P.C. & Kawana, A. (1993) Simultaneous measurement of intracellular calcium and electrical activity from patterned neural networks in culture. IEEE Trans. Biomed. Eng. 40, 804–10.
Kandler, K. & Katz, L.C. (1995) Neuronal coupling and uncoupling in the developing nervous system. Curr. Opin. Neurobiol. 5, 98–105.
Katz, L.C. (1993) Coordinate activity in retinal and cortical development. Curr. Opin. Neurobiol. 3, 93–9.
Katz, L.C. & Dalva, M.B. (1994) Scanning laser photo-stimulation: a new approach for analyzing brain circuits. J. Neurosci. Methods 54, 205–18.
Lipton, S.A. & Kater, S.B. (1989) Neurotransmitter regulation of neuronal outgrowth, plasticity and survival. Trends Neurosci. 12, 265–70.
Maeda, E., Robinson, H.P. & Kawana, A. (1995) The mechanism of generation and propagation of synchronous bursting in developing networks of cortical neurons. J. Neurosci. 15, 6834–45.
Meister, M., Wong, R.O.L., Baylor, D.A. & Shatz, C.J. (1991) Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Multineuronal recording in vitro 227 Science 252, 939–43.
Meister, M., Pine, J. & Baylor, D.A. (1994) Multi-neuronal signals from the retina: acquisition and analysis. J. Neurosci. Methods 51, 95–106.
Meister, M., Lagnado, L. & Baylor, D.A. (1995) Concerted signalling by retinal ganglion cells. Science 270, 1207–10.
Nelson, D.A. & Katz, L.C. (1995) Emergence of functional circuits in ferret visual cortex visualized by optical imaging. Neuron 15, 23–34.
Novak, J.L. & Wheeler, B.C. (1988) Multisite hippocampal slice recording and stimulation using a 32 element micorelectrode array. J. Neurosci. Methods 23, 149–59.
O'donovan, M., Ho, S. & Yee, W. (1994) Calcium imaging of rhythmic network activity in the developing spinal cord of the chick embryo. J. Neurosci. 14, 6354–69.
Pine, J. (1980) Recording action potentials from cultured neurons with extracellular microcircuit electrodes. J. Neurosci. Methods 2, 19–31.
Regehr, W.G. & Atluri, P.P. (1995) Caclium transients in cerebellar granule cell presynaptic terminals. Biophys. J. 68, 2156–70.
Regehr, W.G. & Tank, D.W. (1991) Selective fura-2 loading of presynaptic terminals and nerve cell processes by local perfusion in mammalian brain slice. J. Neurosci. Methods 37, 111–19.
Regehr, W.G., Pine, J., Cohan, C. S., Mischke, M.D. & Tank, D.W. (1989) Sealing cultured invertebrate neurons to embedded dish electrodes facilitates long-term stimulation and recording. J. Neurosci. Methods 30, 91–106.
Robinson, H.P., Kawahara, M., Jimbo, Y., Torimitsu, K., Kuroda, Y. & Kawana, A. (1993) Periodic synchronous bursting and intracellular calcium transients elicited by low Mg2+ in cultured cortical neurons. J. Neurophysiol. 70, 1606–16.
Shuttleworth, T.J. & Thompson, J.L. (1991) Effect of temperature on receptor-activated changes in [Ca2+]i and their determination using fluorescent probes. J. Biol. Chem. 256, 1410–14.
Spitzer, N.C. (1994) Spontaneous calcium spikes and waves in embryonic neurons: signalling systems for differentiation. Trends Neurosci. 17, 155–18.
Tsien, R.Y. (1989) Fluorescent probes of cell signalling. Annu. Rev. Neurosci. 12, 227–53.
Tsien, R.Y. & Poenie, M. (1986) Fluorescence ratio imaging: a new window into intracellular ionic signalling. Trends. Biochem Sci. 11, 450–5.
Tsien, R.Y., Rink, T.J. & Poenie, M. (1985) Measurement of cytosolic free Ca2+ in individual small cells using fluorescence microscopy with dual excitation wavelength. Cell. Caclium 6, 145–57.
Vaney, D. I. (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin. Neurosci. Lett. 125, 187–90.
Williams, D.A., Cody, S.H. & Dubbin, P.N. (1993) Introducing and calibrating fluorescent probes in cells and organelles. In Fluorescent and Luminescent Probes for Biological Activity. (edited by Mason, W.T.), pp. 320–34. London: Academic Press.
Wong, R.O.L. (1993) The role of spatio-temporal firing patterns in neuronal development of sensory systems. Curr. Opin. Neurobiol. 3, 595–601.
Wong, R.O.L. (1995a) Cholinergic regulation of [Ca2+]i during cell division and differentiation in the mammalian retina. J. Neurosci. 15, 2696–706.
Wong, R.O.L. (1995b) Effects of glutamate and its analogs on intracellular calcium levels in the developing retina. Visual Neurosci. 12, 907–17.
Wong, R.O.L. & Oakley, D.M. (1996) Changing patterns of spontaneous bursting activity of On and Off retinal ganglion cells during development. Neuron 16, 1087–95.
Wong, R.O.L., Meister, M. & Shatz, C.J. (1993) Transient period of correlated bursting activity during development of the mammalian retina. Neuron 11, 1–20.
Wong, R.O.L., Chernjavsky, A., Smith, S.J. & Shatz, C.J. (1995) Early functional neural networks in the developing retina. Nature 374, 716–18.
Yuste, R. & Katz, L.C. (1991) Control of postsynaptic Ca2+ influx in developing neocortex by excitatory and inhibitory neurotransmitters. Neuron 6, 333–44.
Yuste, R., Peinado, A. & Katz, L.C. (1992) Neuronal domains in developing neocortex. Science 257, 665–9.
Yuste, R., Nelson, D.A., Rubin, W.W. & Katz, L.C. (1995) Neuronal domains in developing neocortex: mechanism of coactivation. Neuron 14, 7–17.
Suggested reading (optical recordings-dye properties and imaging systems)
Moreton, R.B. (1994) Optical methods for imaging ionic activities. Scanning Microsc. Suppl. 8 371–90.
Mason, W.T. (ed.) (1993) Fluorescent and Luminescent Probes for Biological Activity. London: Academic Press.
Herman, B. & Lemaster, J. (eds) (1993) Optical Microscopy: Emerging Methods and Applications. San Diego: Academic Press.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wong, R.O.L. Calcium imaging and multielectrode recordings of global patterns of activity in the developing nervous system. Histochem J 30, 217–229 (1998). https://doi.org/10.1023/A:1003251504594
Issue Date:
DOI: https://doi.org/10.1023/A:1003251504594