Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex.

1. Voltage and current recordings were made from visually identified non‐pyramidal neurones in slices of layer IV of rat primary visual cortex using the whole‐cell configuration of the patch clamp technique. These neurones are characterized by a high input resistance (0.5‐2 G omega) and a non‐adaptive behaviour of action potential frequency following depolarizing current injection, which suggests that they are stellate cells. 2. Excitatory postsynaptic currents (EPSCs) were recorded from these neurones during focal stimulation of neighbouring cells by a second patch pipette, the tip of which was placed on the soma of the stimulated cell. The response amplitude as a function of stimulus strength showed a sharp increase at a critical stimulus strength suggesting that stimulus‐evoked currents represent unitary EPSCs. 3. In most cases the latencies of stimulus‐evoked EPSCs were unimodally distributed with means in the range of 2.1‐3.6 ms. In some experiments two peaks were seen in the distribution of latencies. The EPSC rise times, measured as the time from 20 to 80% peak amplitude, fell into a distribution ranging from 0.1 to 0.8 ms with a peak at 0.2 ms. The EPSC decay time course at ‐70 mV membrane potential was fitted by a single exponential with a time constant of 2.39 +/‐ 0.99 ms (mean +/‐ S.D.). The rise and decay times were independent of EPSC peak amplitudes. 4. The peak amplitude of successive unitary EPSCs, elicited by a constant stimulus, fluctuated at random. At a holding potential of ‐70 mV the peak amplitudes varied between 5 and 90 pA. In two out of ten cells the histogram of peak amplitudes could be well fitted by the sum of several equidistant Gaussians with a peak distance of around 10 pA. This suggests that the quantal conductance change underlying the peak current fluctuations is of the order of 100 pS. 5. At membrane potentials more positive than ‐70 mV the decay of stimulus‐evoked EPSCs showed two components with very different time courses. In standard extracellular solution the current‐voltage (I‐V) relation for the fast component was almost linear whereas the slow component showed a J‐shaped I‐V relation with a region of negative slope conductance between ‐30 and ‐70 mV.(ABSTRACT TRUNCATED AT 400 WORDS)

[1]  W. Krieg.  Connections of the cerebral cortex. I. The albino rat. A. Topography of the cortical areas , 1946 .

[2]  Walle J. H. Nauta,et al.  Connections of the Cerebral Cortex , 1964 .

[3]  A. Peters,et al.  An autoradiographic study of the projections from the lateral geniculate body of the rat , 1975, Brain Research.

[4]  K Zilles,et al.  A quantitative approach to cytoarchitectonics. VI. The areal pattern of the cortex of the albino rat. , 1980, Anatomy and embryology.

[5]  T. Powell,et al.  An electron microscopic study of the types and proportions of neurons in the cortex of the motor and visual areas of the cat and rat. , 1980, Brain : a journal of neurology.

[6]  J. Collins,et al.  Phosphonate analogues of carboxylic acids as aminoacid antagonists on rat cortical neurones , 1981, Neuroscience Letters.

[7]  R. H. Evans,et al.  THE EFFECTS OF A SERIES OF ω‐PHOSPHONIC α‐CARBOXYLIC AMINO ACIDS ON ELECTRICALLY EVOKED AND EXCITANT AMINO ACID‐INDUCED RESPONSES IN ISOLATED SPINAL CORD PREPARATIONS , 1982 .

[8]  S J Redman,et al.  The synaptic current evoked in cat spinal motoneurones by impulses in single group 1a axons. , 1983, The Journal of physiology.

[9]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. II. Quantitative analysis , 1983, Journal of neurocytology.

[10]  L. Nowak,et al.  Magnesium gates glutamate-activated channels in mouse central neurones , 1984, Nature.

[11]  P. Streit.  Glutamate and Aspartate as Transmitter Candidates for Systems of the Cerebral Cortex , 1984 .

[12]  M. Mayer,et al.  Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones , 1984, Nature.

[13]  J R Wolff,et al.  Postnatal development of axosomatic synapses in the rat visual cortex: Morphogenesis and quantitative evaluation , 1985, The Journal of comparative neurology.

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

[15]  A. Thomson,et al.  An N-methylaspartate receptor-mediated synapse in rat cerebral cortex: a site of action of ketamine? , 1985, Nature.

[16]  A. Thomson.  A magnesium‐sensitive post‐synaptic potential in rat cerebral cortex resembles neuronal responses to N‐methylaspartate. , 1986, The Journal of physiology.

[17]  C. Koch,et al.  Neuronal connections underlying orientation selectivity in cat visual cortex , 1987, Trends in Neurosciences.

[18]  S. Cull-Candy,et al.  Multiple-conductance channels activated by excitatory amino acids in cerebellar neurons , 1987, Nature.

[19]  C. Stevens,et al.  Glutamate activates multiple single channel conductances in hippocampal neurons , 1987, Nature.

[20]  T. Bliss,et al.  NMDA receptors - their role in long-term potentiation , 1987, Trends in Neurosciences.

[21]  M. W. Brown,et al.  CNQX blocks acidic amino acid induced depolarizations and synaptic components mediated by non-NMDA receptors in rat hippocampal slices , 1988, Neuroscience Letters.

[22]  N. L. Chamberlin,et al.  Amino acid receptors and uptake systems in the mammalian central nervous system. , 1988, Critical reviews in neurobiology.

[23]  S N Davies,et al.  Quinoxalinediones: potent competitive non-NMDA glutamate receptor antagonists. , 1988, Science.

[24]  J. Swann,et al.  N-methyl-d-aspartate (NMDA) receptors are inactivated by trypsin , 1988, Brain Research.

[25]  Karrie R. Jones,et al.  NMDA- and non-NMDA-receptor components of excitatory synaptic potentials recorded from cells in layer V of rat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  S. Hagiwara,et al.  Synaptic transmission between rat cerebellar granule and Purkinje cells in dissociated cell culture: effects of excitatory-amino acid transmitter antagonists. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Roland S. G. Jones.  Epileptiform events induced by GABA-antagonists in entorhinal cortical cells in vitro are partly mediated byN-methyl-d-aspartate receptors , 1988, Brain Research.

[28]  R. Lester,et al.  Synaptic activation of N‐methyl‐D‐aspartate receptors in the Schaffer collateral‐commissural pathway of rat hippocampus. , 1988, The Journal of physiology.

[29]  RW Baughman,et al.  The pharmacology of synapses formed by identified corticocollicular neurons in primary cultures of rat visual cortex , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  C. Stevens,et al.  NMDA and non-NMDA receptors are co-localized at individual excitatory synapses in cultured rat hippocampus , 1989, Nature.

[31]  T. Wiesel,et al.  Pharmacological analysis of cortical circuitry , 1989, Trends in Neurosciences.

[32]  A. Konnerth,et al.  Patch clamp techniques used for studying synaptic transmission in slices of mammalian brain. , 1989, Quarterly journal of experimental physiology.

[33]  S. Grillner,et al.  Excitatory amino acids and synaptic transmission: the evidence for a physiological function. , 1990, Trends in pharmacological sciences.

[34]  B Sakmann,et al.  Quantal analysis of inhibitory synaptic transmission in the dentate gyrus of rat hippocampal slices: a patch‐clamp study. , 1990, The Journal of physiology.

[35]  C. Stevens,et al.  Presynaptic mechanism for long-term potentiation in the hippocampus , 1990, Nature.

[36]  B. Connors,et al.  Intrinsic firing patterns of diverse neocortical neurons , 1990, Trends in Neurosciences.

[37]  R. Nicoll,et al.  Analysis of excitatory synaptic action in pyramidal cells using whole‐cell recording from rat hippocampal slices. , 1990, The Journal of physiology.

[38]  R. Nicoll,et al.  Functional comparison of neurotransmitter receptor subtypes in mammalian central nervous system. , 1990, Physiological reviews.

[39]  E. D'Angelo,et al.  Dual-component NMDA receptor currents at a single central synapse , 1990, Nature.

[40]  A. Konnerth,et al.  Synaptic currents in cerebellar Purkinje cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[41]  R. Tsien,et al.  Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices , 1990, Nature.

[42]  R. Nicoll,et al.  Mechanisms generating the time course of dual component excitatory synaptic currents recorded in hippocampal slices , 1990, Neuron.

[43]  I. Módy,et al.  Differential activation of glutamate receptors by spontaneously released transmitter in slices of neocortex , 1990, Neuroscience Letters.

[44]  T. Tsumoto,et al.  Contribution of quisqualate/ kainate and NMDA receptors to excitatory synaptic transmission in the rat's visual cortex , 1990, Visual Neuroscience.

[45]  G. Westbrook,et al.  Channel kinetics determine the time course of NMDA receptor-mediated synaptic currents , 1990, Nature.

[46]  Tadaharu Tsumoto,et al.  Excitatory amino acid transmitters and their receptors in neural circuits of the cerebral neocortex , 1990, Neuroscience Research.

[47]  V. Braitenberg,et al.  Classification of Cortical Neurons , 1991 .

[48]  K. Stratford,et al.  Quantal analysis of excitatory synaptic action and depression in hippocampal slices , 1991, Nature.