Origins of the variations in long-term potentiation between synapses in the basal versus apical dendrites of hippocampal neurons

Abstract

Responses to theta pattern stimulation, and the long-term potentiation (LTP) they induce, were compared in the basal versus apical dendrites of neurons in field CA1 of hippocampus. A series of 10 theta bursts produced more than twice as much LTP in basal synapses as in their apical counterparts as measured with field EPSPs. This confirms earlier field potential studies showing that the maximum degree of potentiation (the LTP ceiling) is considerably greater in stratum oriens than stratum radiatum. Experiments with whole-cell clamp recording obtained similar results, indicating that synapses at different loci on the same neuron reach different LTP ceilings following prolonged theta burst stimulation. The basal synapses also required fewer theta bursts to reach their LTP ceiling than did the apical synapses. Tests with paired-pulse facilitation and an antagonist of the NMDA receptor gave no indication that the greater LTP in basal synapses was qualitatively different from the lesser effect obtained in apical contacts. Intracellular recording revealed significant differences between basal versus apical responses to single theta bursts and trains of bursts: the within-burst depolarization was greater and the between-burst hyperpolarization was smaller for the basal dendritic responses. These two variables have previously been proposed to influence the magnitude of LTP and the observed differences between basal versus apical synapses are in accord with this hypothesis. Together with recently described immunocytochemical results, the findings reported here suggest that variations in LTP across dendritic subfields of hippocampus reflect a differential distribution of a subclass of GABAergic interneurons.