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The Journal of Neurophysiology Vol. 86 No. 6 December 2001, pp. 2973-2985
Copyright ©2001 by the American Physiological Society
Department of Neurology and Neurological Sciences, Stanford University Medical Center, Stanford, California 94305-5122
Kumar, Sanjay S. and
John R. Huguenard.
Properties of Excitatory Synaptic Connections Mediated by the
Corpus Callosum in the Developing Rat Neocortex. J. Neurophysiol. 86: 2973-2985, 2001. 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 
-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 µM) 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
~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 Pr 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.
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