The Functional Influence of Burst and Tonic Firing Mode on Synaptic Interactions in the Thalamus

Thalamocortical and perigeniculate (PGN) neurons can generate action potentials either as Ca2+ spike–mediated high-frequency bursts or as tonic trains. Using dual intracellular recordings in vitro in monosynaptically connected pairs of PGN and dorsal lateral geniculate nucleus (LGNd) neurons, we found that the functional effect of synaptic transmission between these cell types was strongly influenced by the membrane potential and hence the firing mode of both the pre- and postsynaptic neurons. Activation of single action potentials or low-frequency spike trains in PGN or thalamocortical neurons resulted in the generation of PSPs that were 0.5–2.0 mV in amplitude. In contrast, the generation of Ca2+ spike-mediated bursts of action potentials in the presynaptic cell increased these PSPs to an average of 4.4 mV for the IPSP and 3.0 mV for the EPSP barrage, because of temporal summation and/or facilitation. If the postsynaptic neuron was at a resting membrane potential (e.g., −65 mV), these PSP barrages could result in the activation of a low-threshold Ca2+ spike and burst of action potentials. These results demonstrate that the burst firing mode of action potential generation is a particularly effective means by which perigeniculate and thalamocortical neurons may influence one another. We propose that the activation of burst discharges in these cell types is essential for the generation of some forms of synchronized rhythmic oscillations of sleep and of epileptic seizures.

[1]  B. Bean,et al.  GABAB Receptor-Activated Inwardly Rectifying Potassium Current in Dissociated Hippocampal CA3 Neurons , 1996, The Journal of Neuroscience.

[2]  Thomas J. Carew,et al.  Multiple overlapping processes underlying short-term synaptic enhancement , 1997, Trends in Neurosciences.

[3]  R. Nicoll,et al.  Local and diffuse synaptic actions of GABA in the hippocampus , 1993, Neuron.

[4]  J. Deuchars,et al.  Large, deep layer pyramid-pyramid single axon EPSPs in slices of rat motor cortex display paired pulse and frequency-dependent depression, mediated presynaptically and self-facilitation, mediated postsynaptically. , 1993, Journal of neurophysiology.

[5]  S. Lindström,et al.  Private inhibitory systems for the X and Y pathways in the dorsal lateral geniculate nucleus of the cat. , 1990, The Journal of physiology.

[6]  R. Nicoll,et al.  Pre- and postsynaptic GABAB receptors in the hippocampus have different pharmacological properties , 1988, Neuron.

[7]  K. H. Lee,et al.  Modulation of spindle oscillations by acetylcholine, cholecystokinin and 1S,3R-ACPD in the ferret lateral geniculate and perigeniculate nuclei in vitro , 1997, Neuroscience.

[8]  B. Sakmann,et al.  Action of brief pulses of glutamate on AMPA/kainate receptors in patches from different neurones of rat hippocampal slices. , 1992, The Journal of physiology.

[9]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[10]  R. S. Zucker,et al.  Calcium and transmitter release , 1993, Journal of Physiology-Paris.

[11]  R. Miles,et al.  Excitatory synaptic interactions between CA3 neurones in the guinea‐pig hippocampus. , 1986, The Journal of physiology.

[12]  D. McCormick,et al.  What Stops Synchronized Thalamocortical Oscillations? , 1996, Neuron.

[13]  L. Ide,et al.  The fine structure of the perigeniculate nucleus in the cat , 1982, The Journal of comparative neurology.

[14]  Maria V. Sanchez-Vives,et al.  Are the Interlaminar Zones of the Ferret Dorsal Lateral Geniculate Nucleus Actually Part of the Perigeniculate Nucleus? , 1996, The Journal of Neuroscience.

[15]  G Rizzolatti,et al.  Spontaneous activity of neurones of nucleus reticularis thalami in freely moving cats , 1970, The Journal of physiology.

[16]  D. McCormick,et al.  Control of firing mode of corticotectal and corticopontine layer V burst-generating neurons by norepinephrine, acetylcholine, and 1S,3R- ACPD , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  R. Nicoll,et al.  A physiological role for GABAB receptors in the central nervous system , 1988, Nature.

[18]  S. Lindstro¨m Synaptic organization of inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat , 1982, Brain Research.

[19]  P. Somogyi,et al.  Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat , 1983, Neuroscience.

[20]  Steven W. Johnson,et al.  Bicuculline methiodide potentiates NMDA-dependent burst firing in rat dopamine neurons by blocking apamin-sensitive Ca2+-activated K+ currents , 1997, Neuroscience Letters.

[21]  D Debanne,et al.  Physiology and pharmacology of unitary synaptic connections between pairs of cells in areas CA3 and CA1 of rat hippocampal slice cultures. , 1995, Journal of neurophysiology.

[22]  L. Trussell,et al.  Glutamate receptor desensitization and its role in synaptic transmission , 1989, Neuron.

[23]  P. Schwartzkroin,et al.  Electrophysiology of Hippocampal Neurons , 1987 .

[24]  W. A. Wilson,et al.  GABAB autoreceptors mediate activity-dependent disinhibition and enhance signal transmission in the dentate gyrus. , 1993, Journal of neurophysiology.

[25]  M. Steriade,et al.  Reticularis thalami neurons revisited: activity changes during shifts in states of vigilance , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[26]  J. Lambert,et al.  Depression of the fast IPSP underlies paired-pulse facilitation in area CA1 of the rat hippocampus. , 1991, Journal of neurophysiology.

[27]  Adam M. Sillito,et al.  The influence of GABAergic inhibitory processes on the receptive field structure of X and Y cells in cat dorsal lateral geniculate nucleus (dLGN) , 1983, Brain Research.

[28]  K. Horikawa,et al.  A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates , 1988, Journal of Neuroscience Methods.

[29]  D. McCormick,et al.  Sleep and arousal: thalamocortical mechanisms. , 1997, Annual review of neuroscience.

[30]  G. Barrionuevo,et al.  Lateral geniculate nucleus unitary discharge in sleep and waking: state- and rate-specific aspects. , 1983, Journal of neurophysiology.

[31]  J. Scuvée-Moreau,et al.  Evidence for a non-GABAergic action of quaternary salts of bicuculline on dopaminergic neurones , 1997, Neuropharmacology.

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

[33]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[34]  I. Módy,et al.  Differential activation of GABAA and GABAB receptors by spontaneously released transmitter. , 1992, Journal of neurophysiology.

[35]  H. Pape,et al.  Contributions of inhibitory mechanisms to the shift responses of X and Y cells in the cat lateral geniculate nucleus. , 1987, The Journal of physiology.

[36]  Massimo Avoli,et al.  Generalized Epilepsy: Neurobiological Approaches , 1990 .

[37]  D. McCormick,et al.  Abolition of Spindle Oscillations by Serotonin and Norepinephrine in the Ferret Lateral Geniculate and Perigeniculate Nuclei In Vitro , 1996, Neuron.

[38]  O. Snead,et al.  Basic mechanisms of generalized absence seizures , 1995, Annals of neurology.

[39]  J. Deuchars,et al.  Single axon excitatory postsynaptic potentials in neocortical interneurons exhibit pronounced paired pulse facilitation , 1993, Neuroscience.

[40]  H. Scharfman,et al.  Selective depression of GABA-mediated IPSPs by somatostatin in area CA1 of rabbit hippocampal slices , 1989, Brain Research.

[41]  Maria V. Sanchez-Vives,et al.  Functional Properties of Perigeniculate Inhibition of Dorsal Lateral Geniculate Nucleus Thalamocortical Neurons In Vitro , 1997, The Journal of Neuroscience.

[42]  G Oakson,et al.  Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[43]  D. McCormick,et al.  Spindle waves are propagating synchronized oscillations in the ferret LGNd in vitro. , 1995, Journal of neurophysiology.

[44]  M. J. Friedlander,et al.  Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. , 1981, Journal of neurophysiology.

[45]  D. Ferster,et al.  The axonal arborizations of lateral geniculate neurons in the striate cortex of the cat , 1978, The Journal of comparative neurology.

[46]  Maria V. Sanchez-Vives,et al.  Inhibitory Interactions between Perigeniculate GABAergic Neurons , 1997, The Journal of Neuroscience.

[47]  Peter Somogyi,et al.  Diverse sources of hippocampal unitary inhibitory postsynaptic potentials and the number of synaptic release sites , 1994, Nature.

[48]  Maria V. Sanchez-Vives,et al.  Functional dynamics of GABAergic inhibition in the thalamus. , 1997, Science.

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

[50]  D. Contreras,et al.  Cellular basis of EEG slow rhythms: a study of dynamic corticothalamic relationships , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[51]  N. Tamamaki,et al.  Hippocampal pyramidal cells excite inhibitory neurons through a single release site , 1993, Nature.

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

[53]  G Scollo-Lavizzari,et al.  [Generalized epilepsy]. , 2020, Therapeutische Umschau. Revue therapeutique.

[54]  W. Guido,et al.  Burst responses in thalamic relay cells of the awake behaving cat. , 1995, Journal of neurophysiology.

[55]  D. McCormick,et al.  Periodicity of thalamic spindle waves is abolished by ZD7288,a blocker of Ih. , 1998, Journal of neurophysiology.

[56]  R. Miles,et al.  Synaptic excitation of inhibitory cells by single CA3 hippocampal pyramidal cells of the guinea‐pig in vitro. , 1990, The Journal of physiology.

[57]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[58]  T. Sejnowski,et al.  G protein activation kinetics and spillover of gamma-aminobutyric acid may account for differences between inhibitory responses in the hippocampus and thalamus. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[59]  S. Sherman,et al.  Morphological and physiological properties of geniculate W-cells of the cat: a comparison with X- and Y-cells. , 1983, Journal of neurophysiology.

[60]  C. Davies,et al.  The physiological regulation of synaptic inhibition by GABAB autoreceptors in rat hippocampus. , 1993, The Journal of physiology.

[61]  Gang Tong,et al.  Multivesicular release from excitatory synapses of cultured hippocampal neurons , 1994, Neuron.

[62]  I. Cohen,et al.  Calcium and transmitter release. , 1985, International review of neurobiology.

[63]  J. Deuchars,et al.  Synaptic interactions in neocortical local circuits: dual intracellular recordings in vitro. , 1997, Cerebral cortex.

[64]  H. Markram,et al.  Redistribution of synaptic efficacy between neocortical pyramidal neurons , 1996, Nature.

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

[66]  D. J. Uhlrich,et al.  GABAergic circuits in the lateral geniculate nucleus of the cat. , 1992, Progress in brain research.

[67]  A L Humphrey,et al.  Morphology and axonal projection patterns of individual neurons in the cat perigeniculate nucleus. , 1991, Journal of neurophysiology.

[68]  Cha-Min Tang,et al.  Saturation of postsynaptic glutamate receptors after quantal release of transmitter , 1994, Neuron.

[69]  J. Huguenard,et al.  Whole-cell voltage-clamp study of the fading of GABA-activated currents in acutely dissociated hippocampal neurons. , 1986, Journal of neurophysiology.

[70]  P. Saggau,et al.  GABAB receptor‐mediated presynaptic inhibition in guinea‐pig hippocampus is caused by reduction of presynaptic Ca2+ influx. , 1995, The Journal of physiology.

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

[72]  D. McCormick,et al.  Role of the ferret perigeniculate nucleus in the generation of synchronized oscillations in vitro. , 1995, The Journal of physiology.

[73]  D. McCormick,et al.  Synaptic and membrane mechanisms underlying synchronized oscillations in the ferret lateral geniculate nucleus in vitro. , 1995, The Journal of physiology.

[74]  M. Scanziani,et al.  Presynaptic inhibition in the hippocampus , 1993, Trends in Neurosciences.

[75]  E. Evarts TEMPORAL PATTERNS OF DISCHARGE OF PYRAMIDAL TRACT NEURONS DURING SLEEP AND WAKING IN THE MONKEY. , 1964, Journal of neurophysiology.

[76]  G. Rizzolatti,et al.  An analysis of the spontaneous activity of lateral geniculate neurons and of optic tract fibers in free moving cats. , 1970, Archives italiennes de biologie.

[77]  I. Mody,et al.  Bridging the cleft at GABA synapses in the brain , 1994, Trends in Neurosciences.

[78]  W. A. Wilson,et al.  The role of GABAB receptor activation in absence seizures of lethargic (lh/lh) mice. , 1992, Science.

[79]  S. Sherman,et al.  Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus , 1984, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[80]  A. Thomson Activity‐dependent properties of synaptic transmission at two classes of connections made by rat neocortical pyramidal axons in vitro , 1997, The Journal of physiology.

[81]  J R Huguenard,et al.  GABAB receptor‐mediated responses in GABAergic projection neurones of rat nucleus reticularis thalami in vitro. , 1996, The Journal of physiology.

[82]  M. Frosch,et al.  Desensitization of GABA-activated currents and channels in cultured cortical neurons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[83]  G Oakson,et al.  Thalamic burst patterns in the naturally sleeping cat: a comparison between cortically projecting and reticularis neurones. , 1986, The Journal of physiology.

[84]  T. Sejnowski,et al.  Heterogeneous Release Properties of Visualized Individual Hippocampal Synapses , 1997, Neuron.

[85]  D. Prince,et al.  Frequency‐dependent depression of inhibition in guinea‐pig neocortex in vitro by GABAB receptor feed‐back on GABA release. , 1989, The Journal of physiology.