Long-term potentiation/depotentiation are accompanied by complex changes in spontaneous unit activity in the hippocampus

Typically, long-term potentiation (LTP) has been assessed as long-lasting changes in field potentials or intracellularly recorded postsynaptic potentials evoked by activation of a set of afferents. In the present experiment, we determined changes in spontaneous unit activity in the dentate gyrus (DG) following high-frequency (HFS) or low-frequency stimulation (LFS) of the medial perforant pathway. Experiments were performed in anesthetized rats. Field potentials and unit recordings were obtained alternatively from the same recording electrode. Of 39 single units isolated (from 25 independent sessions), the spontaneous discharges of 13 units (33%) increased, while 7 units (18%) decreased their discharges following HFS that induced significant LTP of the field potentials. Such opposing modulations of unit discharges following HFS were observed on simultaneously recorded units. LFS applied following HFS also induced bi-directional effects on unit discharges. Of 20 single units isolated from a subset of recordings (12 experiments) to which LFS was applied, 6 units increased and 4 units decreased their discharges. LFS produced a long-lasting (>20 min) depotentiation, to the baseline level, on field potentials in four recording cases. The autocorrelation functions indicated that the isolated unit discharges were comparable to those of the putative DG granule cells and interneurons, shown in previous studies. The results suggest that changes in synaptic efficacy following HFS or LFS produce rather dynamic changes in cell activity in the DG.