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Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex.
J Neurophysiol. 2001 Dec; 86(6):2973-85.JN

Abstract

Despite the major role of excitatory cortico-cortical connections in mediating neocortical activities, little is known about these synapses at the cellular level. Here we have characterized the synaptic properties of long-range excitatory-to-excitatory contacts between visually identified layer V pyramidal neurons of agranular frontal cortex in callosally connected neocortical slices from postnatal day 13 to 21 (P13-21) rats. Midline stimulation of the corpus callosum with a minimal stimulation paradigm evoked inward excitatory postsynaptic currents (EPSCs) with an averaged peak amplitude of 56.5 +/- 5 pA under conditions of whole cell voltage clamp at -70 mV. EPSCs had fixed latencies from stimulus onset and could follow stimulus trains (1-20 Hz) without changes in kinetic properties. Bath application of 2,3-dihydro-6-nitro-7-sulfamoyl-benzo(F)quinoxaline (NBQX) abolished these responses completely, indicating that they were mediated by alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors (AMPARs). Evoked responses were isolated in picrotoxin to yield purely excitatory PSCs, and a low concentration of NBQX (0.1 microM) was used to partially block AMPARs and prevent epileptiform activity in the tissue. Depolarization of the recorded pyramidal neurons revealed a late, slowly decaying component that reversed at approximately 0 mV and was blocked by D-2-amino-5-phosphonovaleric acid. Thus AMPA and N-methyl-D-aspartate receptors (NMDARs) coexist at callosal synapses and are likely to be activated monosynaptically. The peak amplitudes and decay time constants for EPSCs evoked using minimal stimulation (+/-40 mV) were similar to spontaneously occurring sEPSCs. Typical conductances associated with AMPA and NMDAR-mediated components, deduced from their respective current-voltage (I-V) relationships, were 525 +/- 168 and 966 +/- 281 pS, respectively. AMPAR-mediated responses showed age-dependent changes in the rectification properties of their I-V relationships. While I-Vs from animals >P15 were linear, those in the younger (<P16) age group were inwardly rectifying. Although Ca2+ permeability in AMPARs can be correlated with inward rectification, outside-out somatic patches from younger animals were characterized by Ca2+-impermeable receptors, suggesting that somatic receptors might be functionally different from those located at synapses. While the biophysical properties of AMPAR components of callosally-evoked EPSCs were similar to those evoked by stimulation of local excitatory connections, the NMDA component displayed input-specific differences. NMDAR-mediated responses for local inputs were activated at more hyperpolarized holding potentials in contrast with those evoked by callosal stimulation. Paired stimuli used to assay presynaptic release properties showed paired-pulse depression (PPD) in animals <P16, which converted to facilitation (PPF) in older animals, suggesting a developmental transition from low probability of transmitter release to high P(r) at these synapses and/or alterations in the properties of the underlying postsynaptic receptors. Physiologic properties of neocortical e-e connections are thus input specific and subject to developmental changes in their postsynaptic receptors.

Authors+Show Affiliations

Department of Neurology and Neurological Sciences, Stanford University Medical Center, Stanford, California 94305-5122, USA.No affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

11731554

Citation

Kumar, S S., and J R. Huguenard. "Properties of Excitatory Synaptic Connections Mediated By the Corpus Callosum in the Developing Rat Neocortex." Journal of Neurophysiology, vol. 86, no. 6, 2001, pp. 2973-85.
Kumar SS, Huguenard JR. Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. J Neurophysiol. 2001;86(6):2973-85.
Kumar, S. S., & Huguenard, J. R. (2001). Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. Journal of Neurophysiology, 86(6), 2973-85.
Kumar SS, Huguenard JR. Properties of Excitatory Synaptic Connections Mediated By the Corpus Callosum in the Developing Rat Neocortex. J Neurophysiol. 2001;86(6):2973-85. PubMed PMID: 11731554.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Properties of excitatory synaptic connections mediated by the corpus callosum in the developing rat neocortex. AU - Kumar,S S, AU - Huguenard,J R, PY - 2001/12/4/pubmed PY - 2002/1/29/medline PY - 2001/12/4/entrez SP - 2973 EP - 85 JF - Journal of neurophysiology JO - J Neurophysiol VL - 86 IS - 6 N2 - Despite the major role of excitatory cortico-cortical connections in mediating neocortical activities, little is known about these synapses at the cellular level. Here we have characterized the synaptic properties of long-range excitatory-to-excitatory contacts between visually identified layer V pyramidal neurons of agranular frontal cortex in callosally connected neocortical slices from postnatal day 13 to 21 (P13-21) rats. Midline stimulation of the corpus callosum with a minimal stimulation paradigm evoked inward excitatory postsynaptic currents (EPSCs) with an averaged peak amplitude of 56.5 +/- 5 pA under conditions of whole cell voltage clamp at -70 mV. EPSCs had fixed latencies from stimulus onset and could follow stimulus trains (1-20 Hz) without changes in kinetic properties. Bath application of 2,3-dihydro-6-nitro-7-sulfamoyl-benzo(F)quinoxaline (NBQX) abolished these responses completely, indicating that they were mediated by alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors (AMPARs). Evoked responses were isolated in picrotoxin to yield purely excitatory PSCs, and a low concentration of NBQX (0.1 microM) was used to partially block AMPARs and prevent epileptiform activity in the tissue. Depolarization of the recorded pyramidal neurons revealed a late, slowly decaying component that reversed at approximately 0 mV and was blocked by D-2-amino-5-phosphonovaleric acid. Thus AMPA and N-methyl-D-aspartate receptors (NMDARs) coexist at callosal synapses and are likely to be activated monosynaptically. The peak amplitudes and decay time constants for EPSCs evoked using minimal stimulation (+/-40 mV) were similar to spontaneously occurring sEPSCs. Typical conductances associated with AMPA and NMDAR-mediated components, deduced from their respective current-voltage (I-V) relationships, were 525 +/- 168 and 966 +/- 281 pS, respectively. AMPAR-mediated responses showed age-dependent changes in the rectification properties of their I-V relationships. While I-Vs from animals >P15 were linear, those in the younger (<P16) age group were inwardly rectifying. Although Ca2+ permeability in AMPARs can be correlated with inward rectification, outside-out somatic patches from younger animals were characterized by Ca2+-impermeable receptors, suggesting that somatic receptors might be functionally different from those located at synapses. While the biophysical properties of AMPAR components of callosally-evoked EPSCs were similar to those evoked by stimulation of local excitatory connections, the NMDA component displayed input-specific differences. NMDAR-mediated responses for local inputs were activated at more hyperpolarized holding potentials in contrast with those evoked by callosal stimulation. Paired stimuli used to assay presynaptic release properties showed paired-pulse depression (PPD) in animals <P16, which converted to facilitation (PPF) in older animals, suggesting a developmental transition from low probability of transmitter release to high P(r) at these synapses and/or alterations in the properties of the underlying postsynaptic receptors. Physiologic properties of neocortical e-e connections are thus input specific and subject to developmental changes in their postsynaptic receptors. SN - 0022-3077 UR - https://www.unboundmedicine.com/medline/citation/11731554/Properties_of_excitatory_synaptic_connections_mediated_by_the_corpus_callosum_in_the_developing_rat_neocortex_ L2 - https://journals.physiology.org/doi/10.1152/jn.2001.86.6.2973?url_ver=Z39.88-2003&amp;rfr_id=ori:rid:crossref.org&amp;rfr_dat=cr_pub=pubmed DB - PRIME DP - Unbound Medicine ER -