Abstract
Synchronous population activity is present in neuronal networks in both normal conditions1–3 and pathological states such as epilepsy4–8. During early development of the hippocampus, similar bursts are also recorded2,3,9. These spontaneous bursts are generated by the synchronized action of interneurons acting as excitatory cells9. Nevertheless, the mechanism leading to synchronization still remains unclear. Here, we investigate the conditions in which synchronization arises in developing hippocampal networks. Using simultaneous recordings, we demonstrate that bursts result from a local cooperation of active cells within an integration period prior to their onset. During this interval, an increase in the number of excitatory postsynaptic potentials (EPSPs) takes place. By comparing EPSP frequency with burst ocutience we show that bursting takes place in a non-linear, allor-none fashion. This non-linear dependency with EPSP frequency is characterized by a threshold from which synchronized bursting arises (17 Hz) which can be reproduced by extracellular stimulation. We propose that this threshold is a property of the network, and determines the critical frequency at which cellular populations become phase locked. This frequency-threshold mechanism endows hippocampal networks with high-pass filtering behavior. We discuss its functional implication in neuronal computation10, stimulus encoding11–13 and in pathological conditions such as epilepsy5,14.
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References
Meister, M., Wong, R.O.L., Baylor, D.A. and Shatz, C.J. Synchronous bursts of action potentials in ganglion cells of the developing mammalian retina. Science 252, 939–943 (1991)
Ben-Ari, Y., Cherubini, E., Corradetti, R. & Gaiarsa, J.L. Giant synaptic potentials in immature rat CA3 hippocampal neurones. J. Physiol. 416, 303–325 (1989)
Menendez de la Prida, L; Bolea, S & Sanchez-Andres, J. V. Origin of the synchronized network activity in the rabbit developing hippocampus. Eur. J. Neurosci (In press).
Schwartzkroin, P.A. & Price, D.A. Cellular and field potential properties of epileptogenic hippocampal slices, Brain Res 147(1), 117–130 (1978).
Traub, R.D. & Wong, K.S. Cellular mechanism of neuronal synchronization in epilepsy. Science 216, 745–747 (1982).
Wong, R.K.S. & Traub, R.D. Synchronized burst discharge in disinhibited hippocampal slice. I. Initiation in CA2-CA3 region. J. Neurophysiol. 49(2) 442–458 (1983)
Traub, R.D., Miles, R. & Wong, R.K.S. Model of the origin of rhythmic population oscillations in the hippocampal slice. Science 243, 1319–1325, (1989).
Miles, R., Traub, R.D. & Wong, R.K.S. Spread of synchronous firing in longitudinal slices from the CA3 region of the hippocampus. J. Neurophysiol 60(4), 1481–1494 (1988).
Cherubini, E., Gaiarsa, J.L. & Ben-Ari, Y. GABA: an excitatory neurotransmitter in early postnatal life. TINS 14, 615–519 (1991).
Grossberg, S. Nonlinear neural networks: Principles, mechanisms and architectures. Neural Networks 1, 17–61 (1988).
Gray, C.M. & Singer, W. Stimulus specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad. Sci USA 91, 669–674 (1989).
Laurent, G. & Davidowitz, H. Encoding of olfactory information with oscillating neural assemblies. Science 265, 1872–1875 (1994)
Soltesz, I. & Deschenes, M. Low-and high-frequency membrane potential oscillations during theta activity in CA1 and CA3 pyramidal neurons of the rat hippocampus under ketamine-xylazine anesthesia. J. Neurophysiol, 70, 97–116 (1993).
Chamberlin, N.L., Traub, R.D. & Dingledine, R. Role of EPSPs in initiation of spontaneous synchronized burst firing in rat hippocampal neurons bathed in high potassium. J. Neurophysiol 64 (3) 1000–1008 (1990)
Miles, R., Wong, R.K.S & Traub, R.D. Synchronized afterdischarges in the hippocampus: contribution of local synaptic interactions. Neuroscience 12, 1179–1189 (1984).
Bolea, S, Menendez de la Prida, L. & Sanchez-Andres, J.V. GABAA sensitivity along early postnatal development in rabbit. J. Physiol. 493.P., 30S (1996)
Khazipov, R., Leinekugel, X., Khalilov, I., Gaiarsa, J.L. and Ben-Ari, Y. Synchronization of GABAergic interneuronal networks in CA3 subfield of neonatal rat hippocampal slices. J. Physiol 498, 763–772 (1997).
Menendez de la Prida, L, Bolea, S & Sanchez-Andres, J.V. Analytical characterization of spontaneous activity evolution during hippocampal development in the rabbit. Neurosci. Lett 218, 185–187 (1996).
Menendez de la Prida, L, Stollenwerk, N. & Sanchez-Andres, J.V. Bursting as a source for predictability in biological neural network activity. Physica D, 110, 323–331 (1997).
Treves, A. & Rolls, E.T. Computational analysis of the role of the hippocampus in memory. Hippocampus. 4(3), 374–391 (1994)
Lisman, J.E.. Burst as a unit of neural information: making unreliable synapses reliable. TINS 20, 38–43 (1997).
Cobb, S.R., Buhl, E.H., Halasy, K., Paulsen, O. & Somogyi P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 378, 75–78 (1995).
Miles R. & Wong, R. K. S. Single neurones can initiate sychronized population discharge in the hippocampus. Nature 306, 371–373 (1983).
Scharfman, H.E. Dentate hilar cells with dendrites in the molecular layer have lower threshold for synaptic activation by perforant path than granule cells. J. Neurosci. 11(6) 1660–1673 (1991).
Lacaille, J.C. Mueller, A.L., Dennis D.K. & Schwartzkroin, P.A. Local circuit interactions between oriens/alveus interneurons and CA1 pyramidal cells in hippocampal slices: electrophysiology and morphology. J. Neurosci. 7(7), 1979–1993 (1987)
Wong, R.K.S. & Prince, D.A. Afterpotential generation in hippocampal pyramidal cells. J. Neurophysiol. 45(1):86–97 (1981).
Schwartzkroin, P.A., Moshé, S.L. Noebels, J.L. & Swann, J.W. in Brain Development and Epilepsy. (Oxford Univ. Press, 1995).
Stopfer, M., Bhagavan, S., Smith, B.H. & Laurent, G. Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390, 70–74 (1997).
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de la Prida, L.M., Sanchez-Andres, J.V. (1999). Filtering capability of neural networks from the developing mammalian hippocampus. In: Mira, J., Sánchez-Andrés, J.V. (eds) Foundations and Tools for Neural Modeling. IWANN 1999. Lecture Notes in Computer Science, vol 1606. Springer, Berlin, Heidelberg. https://doi.org/10.1007/BFb0098163
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DOI: https://doi.org/10.1007/BFb0098163
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