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Journal of Neuroscience, Vol 14, 1775-1788, Copyright © 1994 by Society for Neuroscience
Paired pulse depression in cultured hippocampal neurons is due to a presynaptic mechanism independent of GABAB autoreceptor activation
KS Wilcox and MA Dichter
Department of Physiology, University of Pennsylvania, School of Medicine, Philadelphia 19104.
Most rapid synaptic inhibition in the vertebrate forebrain is mediated by
GABA acting via GABAA and GABAB postsynaptic receptors. GABAergic
neurotransmission exhibits frequency-dependent modulation; sequential
inhibitory post-synaptic currents (IPSCs) evoked with interstimulus
intervals between 25 msec and 4 sec routinely result in the attenuation of
the amplitude of the second IPSC. This form of synaptic plasticity is known
as paired pulse depression (PPD). The mechanism of PPD is presently unknown
and the experiments performed in this study were designed to determine
directly the location of the mechanism of PPD in hippocampal neurons
maintained in low-density tissue culture. Evoked IPSCs were recorded
between pairs of cultured neurons grown in relative isolation that were
simultaneously being recorded with the whole-cell, patch-clamp technique.
It was therefore possible to measure miniature IPSCs (mIPSCs) originating
from the same synapses that were being stimulated to evoke release. PPD
occurred routinely in this system, but the amplitudes of mIPSCs following
IPSCs were unchanged. These results indicate that a presynaptic mechanism
mediates PPD. The inability of GABAB receptor antagonists to block PPD
revealed that this form of presynaptic plasticity was not due to
autoinhibition of transmitter release via activation of presynaptic GABAB
receptors. However, manipulations that significantly lowered the
probability of release of neurotransmitter during the first action
potential of a trial (e.g., lower calcium or baclofen) prevented the
development of PPD. These results indicate that, under baseline conditions,
the quantal content for IPSCs is relatively large for a single action
potential, but the quantal content rapidly decreases, such that subsequent
action potentials consistently result in much smaller IPSCs for periods as
long as 4 sec.
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