Developmental alterations in the functional properties of excitatory neocortical synapses

In the neocortex, most excitatory, glutamatergic synapses are established during the first 4–5 weeks after birth. During this period profound changes in the properties of synaptic transmission occur. Excitatory postsynaptic potentials (EPSPs) at immature synaptic connections are profoundly and progressively reduced in response to moderate to high frequency (5–100 Hz) stimulation. With maturation, this frequency‐dependent depression becomes progressively weaker and may eventually transform into a weak to moderate EPSP facilitation. In parallel to changes in the short‐term plasticity, a reduction in the synaptic reliability occurs at most glutamatergic neocortical synapses: immature synapses show a high probability of neurotransmitter release as indicated by their low failure rate and small EPSP amplitude variation. This high reliability is reduced in mature synapses, which show considerably higher failure rates and more variable EPSP amplitudes. During early neocortical development synaptic vesicle pools are not yet fully differentiated and their replenishment may be slow, thus resulting in EPSP amplitude depression. The decrease in the probability of neurotransmitter release may be the result of an altered Ca2+ control in the presynaptic terminal with a reduced Ca2+ influx and/or a higher Ca2+ buffering capacity. This may lead to a lower synaptic reliability and a weaker short‐term synaptic depression with maturation.

[1]  B. Sakmann,et al.  Transmitter release modulation by intracellular Ca2+ buffers in facilitating and depressing nerve terminals of pyramidal cells in layer 2/3 of the rat neocortex indicates a target cell‐specific difference in presynaptic calcium dynamics , 2001, The Journal of physiology.

[2]  A. Reyes,et al.  Nicotinic and Muscarinic Reduction of Unitary Excitatory Postsynaptic Potentials in Sensory Cortex; Dual Intracellular Recording in Vitro Slice Preparation and Recording , 2022 .

[3]  Yildirim Sara,et al.  Development of Vesicle Pools during Maturation of Hippocampal Synapses , 2002, The Journal of Neuroscience.

[4]  W. Regehr,et al.  Short-term synaptic plasticity. , 2002, Annual review of physiology.

[5]  M. Celio,et al.  Calbindin D-28k and parvalbumin in the rat nervous system , 1990, Neuroscience.

[6]  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.

[7]  P. Somogyi,et al.  Target-cell-specific facilitation and depression in neocortical circuits , 1998, Nature Neuroscience.

[8]  Henry Markram,et al.  Synaptic pathways in neural microcircuits , 2005, Trends in Neurosciences.

[9]  Karel Svoboda,et al.  Experience-dependent and cell-type-specific spine growth in the neocortex , 2006, Nature.

[10]  D. Jones,et al.  Quantitation of terminal parameters and their interrelationships in maturing central synapses: A perspective for experimental studies , 1980, Brain Research.

[11]  Jinhyung Kim,et al.  Actin/α-Actinin-Dependent Transport of AMPA Receptors in Dendritic Spines: Role of the PDZ-LIM Protein RIL , 2004, The Journal of Neuroscience.

[12]  H. von Gersdorff,et al.  Fine-Tuning an Auditory Synapse for Speed and Fidelity: Developmental Changes in Presynaptic Waveform, EPSC Kinetics, and Synaptic Plasticity , 2000, The Journal of Neuroscience.

[13]  K. Svoboda,et al.  Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex , 2002, Nature.

[14]  E G Jones,et al.  Inhibitory synaptogenesis in mouse somatosensory cortex. , 1997, Cerebral cortex.

[15]  H. Monyer,et al.  NR2A Subunit Expression Shortens NMDA Receptor Synaptic Currents in Developing Neocortex , 1997, The Journal of Neuroscience.

[16]  K. Svoboda,et al.  Cell Type-Specific Structural Plasticity of Axonal Branches and Boutons in the Adult Neocortex , 2006, Neuron.

[17]  C. Pouzat,et al.  Developmental Regulation of Basket/Stellate Cell→Purkinje Cell Synapses in the Cerebellum , 1997, The Journal of Neuroscience.

[18]  T. Shirao,et al.  Differential expression of rat brain synaptic proteins in development and aging. , 1998, Biochemical and biophysical research communications.

[19]  Andrei Rozov,et al.  Polyamine-dependent facilitation of postsynaptic AMPA receptors counteracts paired-pulse depression , 1999, Nature.

[20]  J. Lübke,et al.  Excitatory signal flow and connectivity in a cortical column: focus on barrel cortex , 2007, Brain Structure and Function.

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

[22]  Michael E. Greenberg,et al.  From Synapse to Nucleus: Calcium-Dependent Gene Transcription in the Control of Synapse Development and Function , 2008, Neuron.

[23]  D. Lovinger,et al.  Decreased probability of neurotransmitter release underlies striatal long-term depression and postnatal development of corticostriatal synapses. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[24]  S. Siegelbaum,et al.  Regulation of hippocampal transmitter release during development and long-term potentiation. , 1995, Science.

[25]  B. Gähwiler,et al.  Target cell-specific modulation of transmitter release at terminals from a single axon. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[26]  F. Bellinger,et al.  Developmentally Regulated Switch in Alternatively Spliced SNAP-25 Isoforms Alters Facilitation of Synaptic Transmission , 2004, The Journal of Neuroscience.

[27]  P. Goldman-Rakic,et al.  Presynaptic regulation of recurrent excitation by D1 receptors in prefrontal circuits. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  S. Iwasaki,et al.  Developmental regulation of transmitter release at the calyx of Held in rat auditory brainstem , 2001, The Journal of physiology.

[29]  Alberto Bacci,et al.  A Developmental Switch of AMPA Receptor Subunits in Neocortical Pyramidal Neurons , 2002, The Journal of Neuroscience.

[30]  R. Schneggenburger,et al.  Developmental expression of the Ca 2 +-binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice , 2004 .

[31]  Zhong-Wei Zhang,et al.  Maturation of layer V pyramidal neurons in the rat prefrontal cortex: intrinsic properties and synaptic function. , 2004, Journal of neurophysiology.

[32]  Yun Wang,et al.  Developmental Switch in the Contribution of Presynaptic and Postsynaptic NMDA Receptors to Long-Term Depression , 2007, The Journal of Neuroscience.

[33]  Bert Sakmann,et al.  Postnatal development of synaptic transmission in local networks of L5A pyramidal neurons in rat somatosensory cortex , 2007, The Journal of physiology.

[34]  J. Lübke,et al.  The morphology of excitatory central synapses: from structure to function , 2006, Cell and Tissue Research.

[35]  L. Abbott,et al.  Synaptic Depression and Cortical Gain Control , 1997, Science.

[36]  W. Gan,et al.  Development of Long-Term Dendritic Spine Stability in Diverse Regions of Cerebral Cortex , 2005, Neuron.

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

[38]  A. Rozov,et al.  Target-Specific Regulation of Synaptic Amplitudes in the Neocortex , 2005, The Journal of Neuroscience.

[39]  B. Katz,et al.  The role of calcium in neuromuscular facilitation , 1968, The Journal of physiology.

[40]  J. Porter,et al.  Adenosine A1 receptors decrease thalamic excitation of inhibitory and excitatory neurons in the barrel cortex , 2006, Neuroscience.

[41]  S. Cohen-Cory.  The Developing Synapse: Construction and Modulation of Synaptic Structures and Circuits , 2002, Science.

[42]  Alex M Thomson,et al.  Excitatory and inhibitory connections show selectivity in the neocortex , 2005, The Journal of physiology.

[43]  James E. Vaughn,et al.  Review: Fine structure of synaptogenesis in the vertebrate central nervous system , 1989 .

[44]  K. Fox,et al.  Presynaptic efficacy directs normalization of synaptic strength in layer 2/3 rat neocortex after paired activity. , 2007, Journal of neurophysiology.

[45]  J R Huguenard,et al.  Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. , 2001, Journal of neurophysiology.

[46]  T. Sejnowski,et al.  Dopamine D1/D5 receptor modulation of excitatory synaptic inputs to layer V prefrontal cortex neurons. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[47]  B. Gustafsson,et al.  Developmental changes in release properties of the CA3-CA1 glutamate synapse in rat hippocampus. , 2004, Journal of neurophysiology.

[48]  T. Sudhof,et al.  The synaptic vesicle cycle. , 2004, Annual review of neuroscience.

[49]  Daniel E Feldman,et al.  Development of Columnar Topography in the Excitatory Layer 4 to Layer 2/3 Projection in Rat Barrel Cortex , 2003, The Journal of Neuroscience.

[50]  M. Seagar,et al.  Developmental Regulation of Synaptotagmin I, II, III, and IV mRNAs in the Rat CNS , 1997, The Journal of Neuroscience.

[51]  H. Luhmann,et al.  Functional Synaptic Projections onto Subplate Neurons in Neonatal Rat Somatosensory Cortex , 2002, The Journal of Neuroscience.

[52]  Alex D. Reyes,et al.  Cholinergic modulation of local pyramid–interneuron synapses exhibiting divergent short-term dynamics in rat sensory cortex , 2008, Brain Research.

[53]  Quanxin Wang,et al.  Multiple Distinct Subtypes of GABAergic Neurons in Mouse Visual Cortex Identified by Triple Immunostaining , 2007, Frontiers in neuroanatomy.

[54]  S. Vicini,et al.  Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons , 1998, The Journal of physiology.

[55]  Katsunori Kobayashi,et al.  Developmental Decrease in Synaptic Facilitation at the Mouse Hippocampal Mossy Fibre Synapse , 2003, The Journal of physiology.

[56]  D. Johnston,et al.  Target Cell-Dependent Normalization of Transmitter Release at Neocortical Synapses , 2005, Science.

[57]  R. Yuste,et al.  Stereotyped position of local synaptic targets in neocortex. , 2001, Science.

[58]  M. C. Angulo,et al.  Developmental Synaptic Changes Increase the Range of Integrative Capabilities of an Identified Excitatory Neocortical Connection , 1999, The Journal of Neuroscience.

[59]  Karel Svoboda,et al.  Precise Development of Functional and Anatomical Columns in the Neocortex , 2004, Neuron.

[60]  B. Sakmann,et al.  Developmental Switch in the Short-Term Modification of Unitary EPSPs Evoked in Layer 2/3 and Layer 5 Pyramidal Neurons of Rat Neocortex , 1999, The Journal of Neuroscience.

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

[62]  M Sur,et al.  Short-term synaptic plasticity in the visual cortex during development. , 1996, Cerebral cortex.

[63]  Xiangrui Li,et al.  Short-term synaptic plasticity in the rat geniculo-cortical pathway during development in vivo , 2006, Neuroscience Letters.

[64]  Alex M. Thomson,et al.  Molecular frequency filters at central synapses , 2000, Progress in Neurobiology.

[65]  J. Huguenard,et al.  Polyamines modulate AMPA receptor-dependent synaptic responses in immature layer v pyramidal neurons. , 2005, Journal of neurophysiology.

[66]  Anne-Marie M Oswald,et al.  Maturation of intrinsic and synaptic properties of layer 2/3 pyramidal neurons in mouse auditory cortex. , 2008, Journal of neurophysiology.

[67]  Xiang Li,et al.  Facilitation versus depression in cultured hippocampal neurons determined by targeting of Ca2+ channel Cavβ4 versus Cavβ2 subunits to synaptic terminals , 2007, The Journal of cell biology.

[68]  P. J. Sjöström,et al.  Multiple forms of long-term plasticity at unitary neocortical layer 5 synapses , 2007, Neuropharmacology.

[69]  J. Huguenard,et al.  Sequential Changes in AMPA Receptor Targeting in the Developing Neocortical Excitatory Circuit , 2008, The Journal of Neuroscience.

[70]  M. Blue,et al.  The formation and maturation of synapses in the visual cortex of the rat. I. Qualitative analysis , 1983, Journal of neurocytology.

[71]  Afia B Ali,et al.  Distinct Ca2+ channels mediate transmitter release at excitatory synapses displaying different dynamic properties in rat neocortex. , 2006, Cerebral cortex.

[72]  B. Connors,et al.  Sensory experience modifies the short-term dynamics of neocortical synapses , 1999, Nature.

[73]  R. Schneggenburger,et al.  Developmental expression of the Ca2+‐binding proteins calretinin and parvalbumin at the calyx of Held of rats and mice , 2004, The European journal of neuroscience.

[74]  H. Markram,et al.  The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[75]  Y. Jan,et al.  Changing subunit composition of heteromeric NMDA receptors during development of rat cortex , 1994, Nature.

[76]  Kristina D. Micheva,et al.  Quantitative aspects of synaptogenesis in the rat barrel field cortex with special reference to GABA circuitry , 1996, The Journal of comparative neurology.

[77]  Moritz Helmstaedter,et al.  Efficient Recruitment of Layer 2/3 Interneurons by Layer 4 Input in Single Columns of Rat Somatosensory Cortex , 2008, The Journal of Neuroscience.

[78]  H. Markram,et al.  Differential signaling via the same axon of neocortical pyramidal neurons. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Noam E. Ziv,et al.  Synapse development: still looking for the forest, still lost in the trees , 2006, Cell and Tissue Research.

[80]  W. Betz,et al.  Synaptic vesicle pools , 2005, Nature Reviews Neuroscience.

[81]  J. Lübke,et al.  Axonal Projection, Input and Output Synapses, and Synaptic Physiology of Cajal–Retzius Cells in the Developing Rat Neocortex , 2002, The Journal of Neuroscience.

[82]  J. E. Vaughn,et al.  Fine structure of synaptogenesis in the vertebrate central nervous system. , 1989, Synapse.

[83]  Daniel Johnston,et al.  Dendritic attenuation of synaptic potentials and currents: the role of passive membrane properties , 1994, Trends in Neurosciences.