A comparison of distal and proximal dendritic synapses on CAi pyramids in guinea-pig hippocampal slices in vitro

J Physiol. 1980 Oct;307:273-99. doi: 10.1113/jphysiol.1980.sp013435.

Abstract

1. In vitro slices of guinea-pig hippocampus have been employed to compare excitatory synapses located distally and proximally on the dendritic tree of CA1 pyramidal cells.2. The main orientation of unmyelinated afferent fibres was found to be parallel to each other and perpendicular to the dendritic axis.3. The density of boutons ending on dendritic spines was roughly similar throughout the greater part of the dendritic tree with an average of 42 +/- 7.2 synapses per 100 mum(2). Their number did, however, decrease in the distal fifth of the apical and in the distal third of the basal dendritic region in parallel with an increase of boutons on the dendritic shafts.4. Negative synaptic field potentials (extracellular field e.p.s.p.s) had their maximum in the region where activated afferent fibres terminated and showed reversal when recorded from sufficiently displaced positions along the dendritic axis. The field e.p.s.p. was preceded by a diphasic presynaptic fibre volley. By cutting all but a narrow bundle of afferent fibres selective activation of a small group of dendritic synapses was possible. Stimulation of fibres crossing tissue bridges (35-100 mum wide) evoked field e.p.s.p.s comparable in amplitude to those seen in slices without lesions. The size of the field e.p.s.p.s evoked via distal and proximal bridges was remarkably similar and linearly related to the size of the appropriate stimulus current and presynaptic volley.5. Selective activation of a small group of afferent fibres gave rise to large amplitude population spikes. Proximal and distal bridges were largely equipotent when they were equally wide. Above the threshold amplitude, the evoked population spikes were linearly related to both the presynaptic volley and the stimulus current. Constant current stimulation of fibres at all apical dendritic levels was equally effective in evoking population spikes, with the exception of the outer fifth of the tree where stimulation was unsuccessful. Input across distal or proximal bridges (400 or 50 mum from the soma) also gave the same high probability of discharge of single units (1.0 for thirty-five of thirty-six cells).6. An input across a narrow and distal bridge (35 mum), representing less than 5% of the fibres synapsing on the apical dendrite, was sufficient to give a firing probability of 1.0 for all cells tested (fifteen).7. For seventeen cells pairs of equally wide distal and proximal apical dendritic bridges were compared. Both inputs gave a mean probability of firing above 0.95 with stimulation strengths less than 2.5 times the spike threshold.8. Intracellular e.p.s.p.s had similar shapes following activation across distal and proximal dendritic bridges. The amplitude of neither type was significantly affected by hyperpolarization of the soma up to 25 mV. The half-width was prolonged to the same moderate degree for both inputs.9. The firing level for the action potential was similar for proximal and distal dendritic inputs and for spikes excited by depolarizing current pulses across the soma membrane.10. The apparent equipotentiality of synchronously activated distal and proximal dendritic synapses is discussed in the light of the known histology of the CA1 pyramidal cells.

Publication types

  • Comparative Study

MeSH terms

  • Action Potentials
  • Animals
  • Dendrites / physiology*
  • Guinea Pigs
  • Hippocampus / physiology*
  • Hippocampus / ultrastructure
  • In Vitro Techniques
  • Neurons, Afferent / physiology
  • Synapses / physiology*