Journal of Neuroscience, Vol 15, 5820-5830, Copyright © 1995 by Society for Neuroscience
Long-term potentiation disrupts auditory gating in the rat hippocampus
CL Miller, PC Bickford, AK Wiser and GM Rose
Department of Pharmacology, University of Colorado Health Sciences Center, Denver 80262, USA.
The consequence of long-term potentiation (LTP) of hippocampal commissural
inputs was investigated in an auditory gating paradigm. Auditory evoked
potentials (AEPs) were recorded in the CA3b region of the hippocampus of
rats anesthesitized with chloral hydrate. Two tones were delivered 0.5 sec
apart; in this paradigm, the second AEP is diminished compared to the
first. Electrical stimulation was applied to hippocampal commissural fibers
to generate field potentials and population spikes which were recorded at
the same site as the AEPs. LTP of the commissural input (initiated by three
trains of 250 Hz/1 sec stimulation) was associated with changes in the
AEPs: on average, the response to the first tone decreased and the response
to the second tone increased, resulting in the disruption of auditory
gating. When high-frequency stimulation of the commissural input failed to
result in LTP, no effect on the AEPs was seen. If
3-(2-carboxypiperazin-4-yl)- propyl-L-phosphonic acid (CPP; 6 mg/kg, i.p.),
an antagonist to the NMDA subclass of glutamate receptors, was administered
prior to high- frequency stimulation, LTP induction was blocked and AEPs
were not affected. Finally, reversal of LTP, achieved by high-frequency
stimulation of CA3 input that was heterosynaptic to the particular
commissural fibers at which the LTP was originally generated, caused
disrupted auditory gating to return to normal. A model of reciprocal LTP
and heterosynaptic depression of commissural and auditory input pathways is
proposed to explain these findings.