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The Journal of Neurophysiology Vol. 87 No. 5 May 2002, pp. 2562-2570
Copyright ©2002 by the American Physiological Society
Departamento de Fisiología, Biofísica y Neurociencias, Centro de Investigación y Estudios Avanzados del Instituto Politécnico Nacional, Mexico D.F. 07000, Mexico
Gutiérrez, Rafael
Activity-Dependent Expression of Simultaneous Glutamatergic and
GABAergic Neurotransmission From the Mossy Fibers In Vitro. J. Neurophysiol. 87: 2562-2570, 2002. GABAergic transmission in the mossy fiber (MF) projection of the
hippocampus is not normally detected in the rat. However, seizures
induce simultaneous glutamatergic and GABAergic transmission in this
projection, which coincides with an overexpression of GAD67 and vesicular GABA transporter (VGAT) mRNA
in the dentate gyrus (DG) and MF. To test whether this plastic change
could be induced in an activity-dependent fashion in the absence of
seizures, I recorded intracellularly from slices/cells that served as
their own control, before and after direct or synaptic kindling of the DG in vitro. As expected, synaptic responses of CA3 pyramidal cells to
test pulse DG stimulation were blocked by perfusion of N-methyl-D-aspartate (NMDA) and non-NMDA
receptors' antagonists. However, after kindling the perforant path (3 1-s trains of 0.1-ms pulses at 100 Hz, 1 min appart from each other
every 15 min for 3 h), which potentiated synaptic responses
without inducing epileptiform activity, the perfusion of glutamatergic
antagonists blocked the excitatory synaptic potential and isolated a
fast bicuculline-sensitive inhibitory synaptic potential.
Immunohistochemical experiments confirmed the overexpression of
GAD67 in the kindled slices. If kindling
stimulation was provided just for 1 h or if it was completed in
the presence of the protein synthesis inhibitor, cycloheximide, the
expression of the GABAergic potential was prevented. Alternatively, when control synaptic responses of a given cell were first blocked, the
direct kindling stimulation over the same site during perfusion of
glutamatergic antagonists resulted in the induction of fast GABAergic
potentials after 16.6 ± 0.9 kindling trials. Furthermore, a high
spacial specificity of this phenomenon was evidenced by recording
synaptic responses of a given pyramidal cell to two different MF
inputs. After blockade of all synaptic responses with the perfusion of
glutamatergic antagonists, one of the inputs was kindled, while
synaptic responses between the kindling trials were monitored by
applying test pulse stimulation to both inputs. After 17 ± 1 trials, test pulse stimulation provided over the kindled site evoked
GABAergic potentials, whereas test pulse stimulation delivered to the
alternative nonkindled parallel MF input remained ineffective. The
DG-evoked GABAergic responses were inhibited by the activation of
GABABR and mGluR, whereby activation of group III
mGluR with L-2-amino-4-phosphonobutyric acid
(L-AP4) was significantly more effective than the
activation of group II mGluR with DCG-IV. These data demonstrate that
GABAergic transmission from the MF projection has distinctive features
in the adult rat, and that its induction is dependent on protein
synthesis responding in an activity-dependent fashion.
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