Plateau Potentials in Cat Neocortical Association Cells In Viva Synaptic Control of Dendritic Excitability

The dendrites of neocortical pyramidal cells are bombarded by myriads of synaptic inputs and express active conductances generating prominent plateau potentials. We have examined in vivo the possibility that spontaneous synaptic inputs trigger or terminate plateau potentials after blockage of K+ currents. Under barbiturate anaesthesia, pairs of cortical cells were intracellularly recorded with sharp electrodes from the cat's association cortex (areas 5–7). In one pyramidal cell, K+ channels were blocked with intracellular Cs+, while in the simultaneously impaled pyramidal cell the K+ conductances were left intact to act as a control; this second cell allowed recognition of spontaneous spindle‐related synaptic activity. Depolarizing current pulses elicited single, all‐or‐none plateau potentials (60–70 mV, 0.1–0.4 s). Plateau potentials slowly repolarized towards a break point of fast repolarization around ‐20 mV. Thalamic‐evoked inhibitory postsynaptic potentials consistently shut off the plateaus. Synchronized spontaneous activity, as occurring during thalamic‐generated spindle oscillations, either triggered or blocked the plateaus. These results suggest that spontaneously occurring synaptic activation during synchronized oscillatory states, such as those that occur during sleep spindles in vivu, may exert a strong control over the dendritic excitability in neocortical pyramidal cells.

[1]  B. Connors,et al.  Apical dendrites of the neocortex: correlation between sodium- and calcium-dependent spiking and pyramidal cell morphology , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  E. G. Jones,et al.  Thalamic oscillations and signaling , 1990 .

[3]  M. Kennedy Regulation of neuronal function by calcium , 1989, Trends in Neurosciences.

[4]  M. Deschenes,et al.  The thalamus as a neuronal oscillator , 1984, Brain Research Reviews.

[5]  B. Connors,et al.  Electrophysiological properties of neocortical neurons in vitro. , 1982, Journal of neurophysiology.

[6]  A. Constanti,et al.  Calcium-dependent action potentials and associated inward currents in guinea-pig neocortical neurons in vitro , 1986, Brain Research.

[7]  M Steriade,et al.  Intracellular analysis of relations between the slow (< 1 Hz) neocortical oscillation and other sleep rhythms of the electroencephalogram , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  R K Wong,et al.  Dendritic mechanisms underlying penicillin-induced epileptiform activity. , 1979, Science.

[9]  A. Destexhe,et al.  Inhibitory control of somatodendritic interactions underlying action potentials in neocortical pyramidal neurons in vivo: An intracellular and computational study , 1998, Neuroscience.

[10]  D Contreras,et al.  Electrophysiological properties of cat reticular thalamic neurones in vivo. , 1993, The Journal of physiology.

[11]  D. McCormick,et al.  Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. , 1985, Journal of neurophysiology.

[12]  B. Connors,et al.  Regenerative activity in apical dendrites of pyramidal cells in neocortex. , 1993, Cerebral cortex.

[13]  M. Deschenes,et al.  Abolition of spindle oscillations in thalamic neurons disconnected from nucleus reticularis thalami. , 1985, Journal of neurophysiology.

[14]  D. Prince,et al.  Intradendritic recordings from hippocampal neurons. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[15]  B. Connors,et al.  Mechanisms of neocortical epileptogenesis in vitro. , 1982, Journal of neurophysiology.

[16]  Barry W. Connors,et al.  Functions of very distal dendrites: experimental and computational studies of layer 1 synapses on neocortical pyramidal cells , 1992 .

[17]  M. Steriade,et al.  Short- and long-range neuronal synchronization of the slow (< 1 Hz) cortical oscillation. , 1995, Journal of neurophysiology.

[18]  R. Llinás,et al.  Electrophysiological properties of dendrites and somata in alligator Purkinje cells. , 1971, Journal of neurophysiology.

[19]  D. Kleinfeld,et al.  In vivo dendritic calcium dynamics in neocortical pyramidal neurons , 1997, Nature.

[20]  M Steriade,et al.  Electrophysiology of cat association cortical cells in vivo: intrinsic properties and synaptic responses. , 1993, Journal of neurophysiology.

[21]  A. Friedman,et al.  Stepwise repolarization from Ca2+ plateaus in neocortical pyramidal cells: evidence for nonhomogeneous distribution of HVA Ca2+ channels in dendrites , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  F. Bezanilla,et al.  Negative Conductance Caused by Entry of Sodium and Cesium Ions into the Potassium Channels of Squid Axons , 1972, The Journal of general physiology.

[23]  D. Prince,et al.  Electrophysiology of isolated hippocampal pyramidal dendrites , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  Rafael Yuste,et al.  Ca2+ accumulations in dendrites of neocortical pyramidal neurons: An apical band and evidence for two functional compartments , 1994, Neuron.

[25]  D. Contreras,et al.  Synchronization of low-frequency rhythms in corticothalamic networks , 1996, Neuroscience.

[26]  W. Calvin Generation of spike trains in CNS neurons , 1975, Brain Research.

[27]  E. Kandel,et al.  ELECTROPHYSIOLOGY OF HIPPOCAMPAL NEURONS: IV. FAST PREPOTENTIALS. , 1961, Journal of neurophysiology.

[28]  R. Llinás The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. , 1988, Science.

[29]  B. Sakmann,et al.  Active propagation of somatic action potentials into neocortical pyramidal cell dendrites , 1994, Nature.

[30]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[31]  R. Llinás,et al.  Electrophysiological properties of in vitro Purkinje cell dendrites in mammalian cerebellar slices. , 1980, The Journal of physiology.

[32]  T. Sejnowski,et al.  Control of Spatiotemporal Coherence of a Thalamic Oscillation by Corticothalamic Feedback , 1996, Science.

[33]  A. Davies,et al.  Intrinsic programmes of growth and survival in developing vertebrate neurons , 1994, Trends in Neurosciences.

[34]  M. Deschenes,et al.  Electrophysiology of neurons of lateral thalamic nuclei in cat: resting properties and burst discharges. , 1984, Journal of neurophysiology.

[35]  P. Schwindt,et al.  Negative slope conductance due to a persistent subthreshold sodium current in cat neocortical neurons in vitro , 1982, Brain Research.

[36]  Wilfrid Rall,et al.  Theoretical significance of dendritic trees for neuronal input-output relations , 1964 .

[37]  D. Purpura,et al.  Properties of synaptic activities and spike potentials of neurons in immature neocortex. , 1965, Journal of neurophysiology.

[38]  D. Prince,et al.  Sodium channels in dendrites of rat cortical pyramidal neurons. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Bartlett W. Mel,et al.  Information Processing in Dendritic Trees , 1994, Neural Computation.

[40]  H. Pockberger,et al.  Electrophysiological and morphological properties of rat motor cortex neurons in vivo , 1991, Brain Research.

[41]  R. Llinás,et al.  Tetrodotoxin-resistant dendritic spikes in avian Purkinje cells. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[42]  K. Maekawa,et al.  Properties of spontaneous and evoked synaptic activities of thalamic ventrobasal neurons. , 1967, Journal of neurophysiology.

[43]  P. Adams The platonic neuron gets the hots , 1992, Current Biology.

[44]  J. Eccles,et al.  Excitatory synaptic action in motoneurones , 1955, The Journal of physiology.

[45]  M. Steriade,et al.  Fast (mainly 30–100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials , 1997, The Journal of physiology.

[46]  D. Prince,et al.  Synaptic control of excitability in isolated dendrites of hippocampal neurons , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[47]  R. Clay Reid,et al.  Visually evoked calcium action potentials in cat striate cortex , 1995, Nature.