Enhanced activation of NMDA receptor responses at the immature retinogeniculate synapse

The maturation of retinogeniculate excitatory transmission and intrathalamic inhibition was studied in slices of the dorsal LGN obtained from ferrets during the first 2 postnatal months. Response to optic tract stimulation at neonatal ages consisted of slow EPSPs lasting several hundred milliseconds. Application of the NMDA receptor antagonist D-(-)-2-amino-5-phosphonovaleric acid (D-APV) during the first 2 postnatal weeks resulted in EPSPs that were reduced in peak amplitude and dramatically curtailed in duration, indicating that NMDA receptors participate strongly in retinogeniculate transmission at the immature synapse. Gradually, EPSPs became shorter in duration such that after the second postnatal week, the retinogeniculate EPSPs were only a few milliseconds in duration. At this late stage of development responses were remarkably less affected by application of D-APV. These changes in contribution of NMDA receptors to retinogeniculate transmission were found to be due to the development of strong IPSPs, the result of gradual maturation of activation of GABAergic inhibition. Indeed, application of bicuculline methiodide to block GABAA receptor- mediated IPSPs strongly enhanced the NMDA component of the EPSPs in more mature cells. The voltage dependence and kinetics of NMDA-induced excitatory postsynaptic currents (NMDA EPSCs) were characterized by voltage-clamp recordings after blocking AMPA/kainate receptors with 6- cyano-7-nitroquinoxaline-2,3-dione and GABAA receptors wit' bicuculline methiodide. The voltage dependence of the NMDA EPSCs remained unaltered with age. During the first postnatal month the kinetic properties of the NMDA EPSCs also remained unaltered, but a reduction in EPSC duration was observed within the following weeks, well after the critical period of anatomical reorganization.(ABSTRACT TRUNCATED AT 250 WORDS)

[1]  T. Verdoorn,et al.  Prenatal ontogeny of the gabaergic system in the rat brain: An immunocytochemical study , 1986, Neuroscience.

[2]  J. K. Harting,et al.  Transient tectogeniculate projections in neonatal kittens: An autoradiographic study , 1985, The Journal of comparative neurology.

[3]  N. A. Buchwald,et al.  Enhanced responses to NMDA receptor activation in the developing cat caudate nucleus , 1991, Neuroscience Letters.

[4]  M. Constantine-Paton,et al.  Patterned activity, synaptic convergence, and the NMDA receptor in developing visual pathways. , 1990, Annual review of neuroscience.

[5]  G. Stent A physiological mechanism for Hebb's postulate of learning. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[6]  L. Haberly,et al.  The development of physiological responses of the piriform cortex in rats to stimulation of the lateral olfactory tract , 1984, The Journal of comparative neurology.

[7]  R. Dingledine,et al.  Regulation of hippocampal NMDA receptors by magnesium and glycine during development. , 1991, Brain research. Molecular brain research.

[8]  C. Shatz,et al.  Synapses formed by identified retinogeniculate axons during the segregation of eye input , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  M. Sur,et al.  Retinogeniculate EPSPs recorded intracellularly in the ferret lateral geniculate nucleus in vitro: Role of NMDA receptors , 1992, Visual Neuroscience.

[10]  Damon L. McCormick,et al.  Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  J. Brunso-Bechtold,et al.  A golgi study of dendritic development in the dorsal lateral geniculate nucleus of normal ferrets , 1991, The Journal of comparative neurology.

[12]  M P Stryker,et al.  On and off sublaminae in the lateral geniculate nucleus of the ferret , 1983, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[13]  W Wisden,et al.  The distribution of thirteen GABAA receptor subunit mRNAs in the rat brain. III. Embryonic and postnatal development , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  A. Kriegstein,et al.  Endogenous neurotransmitter activates N-methyl-D-aspartate receptors on differentiating neurons in embryonic cortex. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[15]  Y. Ben-Ari,et al.  Transient increased density of NMDA binding sites in the developing rat hippocampus , 1988, Brain Research.

[16]  J. Garthwaite,et al.  Selective loss of Purkinje and granule cell responsiveness to N-methyl-D-aspartate in rat cerebellum during development. , 1987, Brain research.

[17]  Shaul Hestrin,et al.  Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse , 1992, Nature.

[18]  M. Sur,et al.  Disruption of retinogeniculate afferent segregation by antagonists to NMDA receptors , 1991, Nature.

[19]  T. Tsumoto,et al.  NMDA receptors in the visual cortex of young kittens are more effective than those of adult cats , 1987, Nature.

[20]  K. Harris,et al.  Evidence for late development of inhibition in area CA1 of the rat hippocampus , 1983, Brain Research.

[21]  A. Fairén,et al.  Differential Expression of the GABAA Receptor Complex in the Dorsal Thalamus and Reticular Nucleus: An Immunohistochemical Study in the Adult and Developing Rat , 1991, The European journal of neuroscience.

[22]  M. Cambray-Deakin,et al.  The expression of excitatory amino acid binding sites during neuritogenesis in the developing rat cerebellum. , 1990, Brain research. Developmental brain research.

[23]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[24]  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.

[25]  M. Stryker,et al.  Prenatal tetrodotoxin infusion blocks segregation of retinogeniculate afferents. , 1988, Science.

[26]  W Singer,et al.  The development of N-methyl-D-aspartate receptors in cat visual cortex. , 1989, Brain research. Developmental brain research.

[27]  J. Wolff,et al.  Development of GABAergic neurons in rat visual cortex as identified by glutamate decarboxylase-like immunoreactivity , 1984, Neuroscience Letters.

[28]  N. Daw,et al.  The location and function of NMDA receptors in cat and kitten visual cortex , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  J. Pettigrew,et al.  Development of single-neuron responses in kitten's lateral geniculate nucleus. , 1978, Journal of neurophysiology.

[30]  P. Rakic Prenatal genesis of connections subserving ocular dominance in the rhesus monkey , 1976, Nature.

[31]  S. Sherman,et al.  N-methyl-D-aspartate receptors contribute to excitatory postsynaptic potentials of cat lateral geniculate neurons recorded in thalamic slices. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  A. Sillito,et al.  The nature of the excitatory transmitter mediating X and Y cell inputs to the cat dorsal lateral geniculate nucleus , 1982, The Journal of physiology.

[33]  J. Taube,et al.  Development of hyperpolarizing inhibitory postsynaptic potentials and hyperpolarizing response to gamma-aminobutyric acid in rabbit hippocampus studied in vitro , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[34]  W. A. Wilson,et al.  Reduced sensitivity of the N-methyl-D-aspartate component of synaptic transmission to magnesium in hippocampal slices from immature rats. , 1990, Brain research. Developmental brain research.

[35]  J. Nadler,et al.  Developmental increase in the sensitivity to magnesium of NMDA receptors on CA1 hippocampal pyramidal cells. , 1990, Brain research. Developmental brain research.

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

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

[38]  M. Pirchio,et al.  Cl‐ ‐ and K+‐dependent inhibitory postsynaptic potentials evoked by interneurones of the rat lateral geniculate nucleus. , 1988, The Journal of physiology.

[39]  A. Agmon,et al.  NMDA receptor-mediated currents are prominent in the thalamocortical synaptic response before maturation of inhibition. , 1992, Journal of neurophysiology.

[40]  Y. Ben-Ari,et al.  Changes in voltage dependence of NMDA currents during development , 1988, Neuroscience Letters.

[41]  J. Hablitz,et al.  Developmental changes in NMDA and non-NMDA receptor-mediated synaptic potentials in rat neocortex. , 1993, Journal of neurophysiology.

[42]  R. Guillery,et al.  The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development , 1981, The Journal of comparative neurology.

[43]  P Heggelund,et al.  Postnatal development of glutamatergic, GABAergic, and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[44]  T. L. Hickey,et al.  An autoradiographic study of retinogeniculate pathways in the cat and the fox , 1974, The Journal of comparative neurology.

[45]  G. Carmignoto,et al.  Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. , 1992, Science.

[46]  Richard Mooney,et al.  Enhancement of transmission at the developing retinogeniculate synapse , 1993, Neuron.

[47]  J. Swann,et al.  Postnatal development of GABA-mediated synaptic inhibition in rat hippocampus , 1989, Neuroscience.