Regulation of the NMDA component of EPSPs by different components of postsynaptic GABAergic inhibition: computer simulation analysis in piriform cortex.

Regulation of the NMDA component of EPSPs by different components of postsynaptic GABAergic inhibition: computer simulation analysis in piriform cortex. J. Neurophysiol. 78: 2546-2559, 1997. Physiological analysis in the companion paper demonstrated that gamma-aminobutyric acid-A (GABAA)-mediated inhibition in piriform cortex is generated by circuits that are largely independent in apical dendritic and somatic regions of pyramidal cells and that GABAA-mediated inhibitory postsynaptic currents (IPSCs) in distal dendrites have a slower time course than those in the somatic region. This study used modeling methods to explore these characteristics of GABAA-mediated inhibition with respect to regulation of the N-methyl--aspartate (NMDA) component of excitatory postsynaptic potentials. Such regulation is relevant to understanding NMDA-dependent long-term potentiation (LTP) and the integration of repetitive synaptic inputs that can activate the NMDA component as well as pathological processes that can be activated by overexpression of the NMDA component. A working hypothesis was that the independence and differing properties of IPSCs in apical dendritic and somatic regions provide a means whereby the NMDA component and other dendritic processes can be controlled by way of GABAergic tone without substantially altering system excitability. The analysis was performed on a branched compartmental model of a pyramidal cell in piriform cortex constructed with physiological and anatomic data derived by whole cell patch recording. Simulations with the model revealed that NMDA expression is more effectively blocked by the slow GABAA component than the fast. Because the slow component is present in greater proportion in apical dendritic than somatic regions, this characteristic would increase the capacity of dendritic IPSCs to regulate NMDA-mediated processes. The simulations further revealed that somatic-region GABAergic inhibition can regulate the generation of action potentials with little effect on the NMDA component generated by afferent fibers in apical dendrites. As a result, if expression of the NMDA component or other dendritic processes were enabled by selective block of dendritic inhibition, for example, by centrifugal fiber systems that may regulate learning and memory, the somatic-region IPSC could preserve system stability through feedback regulation of firing without counteracting the effect of the dendritic-region block. Simulations with paired inputs revealed that the dendritic GABAA-mediated IPSC can regulate the extent to which a strong excitatory input facilitates the NMDA component of a concurrent weak input, providing a possible mechanism for control of "associative LTP" that has been demonstrated in this system. Postsynaptic GABAB-mediated inhibition had less effect on the NMDA component than either the fast or slow GABAA components. Depolarization from a concomitant alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) component also was found to have comparatively little effect on current through the NMDA channel because of its brief time course.

[1]  Arnold R. Kriegstein,et al.  Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex , 1989, Journal of Neuroscience Methods.

[2]  C. Koch,et al.  The dynamics of free calcium in dendritic spines in response to repetitive synaptic input. , 1987, Science.

[3]  M Hines,et al.  A program for simulation of nerve equations with branching geometries. , 1989, International journal of bio-medical computing.

[4]  Robert A. Pearce,et al.  Physiological evidence for two distinct GABAA responses in rat hippocampus , 1993, Neuron.

[5]  N. Spruston,et al.  Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. , 1992, Journal of neurophysiology.

[6]  Lewis B. Haberly,et al.  Associative long-term potentiation in piriform cortex slices requires GABAA blockade , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  W. Lytton,et al.  GABAA-mediated IPSCs in piriform cortex have fast and slow components with different properties and locations on pyramidal cells. , 1997, Journal of neurophysiology.

[8]  D. Johnston,et al.  A Synaptically Controlled, Associative Signal for Hebbian Plasticity in Hippocampal Neurons , 1997, Science.

[9]  Y Yarom,et al.  Voltage behavior along the irregular dendritic structure of morphologically and physiologically characterized vagal motoneurons in the guinea pig. , 1990, Journal of neurophysiology.

[10]  W. Levy,et al.  Blockade of inhibition in a pathway with dual excitatory and inhibitory action unmasks a capability for LTP that is otherwise not expressed , 1990, Brain Research.

[11]  C. Nicholson Electric current flow in excitable cells J. J. B. Jack, D. Noble &R. W. Tsien Clarendon Press, Oxford (1975). 502 pp., £18.00 , 1976, Neuroscience.

[12]  B. Sakmann,et al.  Fast and slow components of unitary EPSCs on stellate cells elicited by focal stimulation in slices of rat visual cortex. , 1992, The Journal of physiology.

[13]  T. Nabeshima Behavioral aspects of cholinergic transmission: role of basal forebrain cholinergic system in learning and memory. , 1993, Progress in brain research.

[14]  G. Lynch,et al.  Benzodiazepines block long-term potentiation in slices of hippocampus and piriform cortex , 1992, Neuroscience.

[15]  D A Turner,et al.  Segmental cable evaluation of somatic transients in hippocampal neurons (CA1, CA3, and dentate). , 1984, Biophysical journal.

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

[17]  E. Adrian Olfactory reactions in the brain of the hedgehog , 1942, The Journal of physiology.

[18]  T. Freund,et al.  Differences between Somatic and Dendritic Inhibition in the Hippocampus , 1996, Neuron.

[19]  C. Scholfield A depolarizing inhibitory potential in neurones of the olfactory cortex in vitro. , 1978, The Journal of physiology.

[20]  D. Prince,et al.  Control of NMDA receptor-mediated activity by GABAergic mechanisms in mature and developing rat neocortex. , 1990, Brain research. Developmental brain research.

[21]  B Sakmann,et al.  Detailed passive cable models of whole-cell recorded CA3 pyramidal neurons in rat hippocampal slices , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[22]  J. D. McGaugh,et al.  Noradrenergic and cholinergic interactions in the amygdala and the modulation of memory storage , 1993, Behavioural Brain Research.

[23]  A. Kapur,et al.  A dendritic GABAA-mediated IPSP regulates facilitation of NMDA-mediated responses to burst stimulation of afferent fibers in piriform cortex , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  W Rall,et al.  Matching dendritic neuron models to experimental data. , 1992, Physiological reviews.

[25]  W Rall,et al.  Estimating the electrotonic structure of neurons with compartmental models. , 1992, Journal of neurophysiology.

[26]  W. Levy,et al.  Insights into associative long-term potentiation from computational models of NMDA receptor-mediated calcium influx and intracellular calcium concentration changes. , 1990, Journal of neurophysiology.

[27]  T. H. Brown,et al.  Associative long-term potentiation in hippocampal slices. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[28]  T. H. Brown,et al.  Biophysical model of a Hebbian synapse. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[29]  B. Sakmann,et al.  Quantal components of unitary EPSCs at the mossy fibre synapse on CA3 pyramidal cells of rat hippocampus. , 1993, The Journal of physiology.

[30]  J. Garthwaite,et al.  Quisqualate neurotoxicity: A delayed, CNQX-sensitive process triggered by a CNQX-insensitive mechanism in young rat hippocampal slices , 1989, Neuroscience Letters.

[31]  L. Haberly,et al.  Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. II. Analysis with a system model. , 1993, Journal of neurophysiology.

[32]  D. Haydon,et al.  Some effects of aliphatic hydrocarbons on the electrical capacity and ionic currents of the squid giant axon membrane. , 1980, The Journal of physiology.

[33]  K L Ketchum,et al.  Synaptic events that generate fast oscillations in piriform cortex , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  L. Haberly,et al.  Membrane currents evoked by afferent fiber stimulation in rat piriform cortex. I. Current source-density analysis. , 1993, Journal of neurophysiology.

[35]  P. Schwindt,et al.  Amplification of synaptic current by persistent sodium conductance in apical dendrite of neocortical neurons. , 1995, Journal of neurophysiology.

[36]  A. Sahgal,et al.  The role of serotonergic-cholinergic interactions in the mediation of cognitive behaviour , 1995, Behavioural Brain Research.

[37]  R. Dingledine,et al.  Involvement of N-methyl-d-aspartate Receptors in Involvement of N-methyl-d-aspartate Receptors in Epileptiform Bursting in the Rat Hippocampal Slice , 2008 .

[38]  W. Levy,et al.  Synapses as associative memory elements in the hippocampal formation , 1979, Brain Research.

[39]  R. Lipowsky,et al.  Dendritic Na+ channels amplify EPSPs in hippocampal CA1 pyramidal cells. , 1996, Journal of neurophysiology.

[40]  J E Lisman,et al.  A model for dendritic Ca2+ accumulation in hippocampal pyramidal neurons based on fluorescence imaging measurements. , 1994, Journal of neurophysiology.

[41]  Gordon M. Shepherd,et al.  Olfactory cortex , 1998 .

[42]  W Rall,et al.  Computational study of an excitable dendritic spine. , 1988, Journal of neurophysiology.

[43]  J. Adams,et al.  Technical considerations on the use of horseradish peroxidase as a neuronal marker , 1977, Neuroscience.

[44]  T. Aigner Pharmacology of memory: cholinergic—glutamatergic interactions , 1995, Current Opinion in Neurobiology.

[45]  William H. Press,et al.  Book-Review - Numerical Recipes in Pascal - the Art of Scientific Computing , 1989 .

[46]  J. Adams Heavy metal intensification of DAB-based HRP reaction product. , 1981, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[47]  Idan Segev,et al.  The Impact of Parallel Fiber Background Activity on the Cable Properties of Cerebellar Purkinje Cells , 1992, Neural Computation.

[48]  S. Sara,et al.  Locus coeruleus-evoked responses in behaving rats: A clue to the role of noradrenaline in memory , 1994, Brain Research Bulletin.

[49]  H. Markram,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997, Science.

[50]  CE Jahr,et al.  A quantitative description of NMDA receptor-channel kinetic behavior , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  W. Singer,et al.  Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex , 1990, Nature.

[52]  D. Perkel,et al.  Quantitative methods for predicting neuronal behavior , 1981, Neuroscience.

[53]  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.

[54]  M. Hasselmo Neuromodulation and cortical function: modeling the physiological basis of behavior , 1995, Behavioural Brain Research.

[55]  D. Thurbon,et al.  Electrotonic profiles of interneurons in stratum pyramidale of the CA1 region of rat hippocampus. , 1994, Journal of neurophysiology.

[56]  T. Gillessen,et al.  Amplification of EPSPs by low Ni(2+)- and amiloride-sensitive Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. , 1997, Journal of neurophysiology.

[57]  O. Steward,et al.  Synaptic inhibition regulates associative interactions between afferents during the induction of long-term potentiation and depression. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[58]  Robert S. Zucker,et al.  Postsynaptic Levels of [Ca2+]i Needed to Trigger LTD and LTP , 1996, Neuron.

[59]  C. Stevens,et al.  Voltage dependence of NMDA-activated macroscopic conductances predicted by single-channel kinetics , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  W. Levy,et al.  Bicuculline permits the induction of long-term depression by heterosynaptic, translaminar conditioning in the hippocampal dentate gyrus , 1993, Brain Research.

[61]  L. Haberly,et al.  Characterization of synaptically mediated fast and slow inhibitory processes in piriform cortex in an in vitro slice preparation. , 1988, Journal of neurophysiology.

[62]  G. Buzsáki,et al.  Interneurons of the hippocampus , 1998, Hippocampus.

[63]  William H. Press,et al.  Numerical recipes in C. The art of scientific computing , 1987 .

[64]  Y. Yaari,et al.  Kinetic properties of NMDA receptor‐mediated synaptic currents in rat hippocampal pyramidal cells versus interneurones. , 1993, The Journal of physiology.

[65]  B. Gustafsson,et al.  Hippocampal long-lasting potentiation produced by pairing single volleys and brief conditioning tetani evoked in separate afferents , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[66]  D. Johnston,et al.  Characterization of single voltage‐gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. , 1995, The Journal of physiology.

[67]  M. Jung,et al.  Further characteristics of long‐term potentiation in piriform cortex , 1994, Synapse.