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Journal of Neuroscience, Vol 13, 3736-3748, Copyright © 1993 by Society for Neuroscience
Occurrence and three-dimensional structure of multiple synapses between individual radiatum axons and their target pyramidal cells in hippocampal area CA1
KE Sorra and KM Harris
Program in Neuroscience, Harvard Medical School, Boston, Massachusetts.
Recent physiological work has used quantal analysis to investigate the
properties of synaptic transmission and long-term potentiation in
hippocampal area CA1. These analyses have revealed changes in the strength
of excitatory post-synaptic responses following long-term potentiation that
could be mediated by cellular mechanisms in the presynaptic element, in the
postsynaptic element, or in both elements. In these studies, either minimal
stimulation, presumably involving a single presynaptic axon, or recordings
from pairs of CA3 and CA1 cells have been used. Interpretation of these
quantal analyses requires knowledge about whether single or multiple
synapses occur between the presynaptic axon and its target CA1 pyramidal
cells. Here, light and serial electron microscopy was used to begin to
examine this question and a related question concerning the ultrastructure
of spines on multiple-synapse boutons. Light microscopic analyses of Golgi
preparations revealed that about 20% of the axons occurring in stratum
radiatum come into close apposition with two to four different dendrites of
a target CA1 cell. An "apposition" was defined as a point where the axons
and dendrites crossed in the same focal plane and therefore were
sufficiently close to allow a dendritic spine to reach the axon and
possibly establish a synaptic contact. An additional 4% of the axons wound
back and forth across individual dendrites, possibly forming multiple
synapses closely spaced along the dendrites. Serial electron microscopy
revealed that 24% of the individual axonal boutons in stratum radiatum make
synapses with multiple dendritic spines arising from either the same or
different dendritic segments. Two adjacent boutons of the same axon could
also be found to synapse with different spines of the same dendrite.
Together with the light microscopic analysis, these observations suggest
that multiple synapses occur between single axons in stratum radiatum and
their target CA1 cells, and that at least some of these synapses may occur
at different electronic distances. If these multiple synapses have
different physiological strengths, then they may obscure or smooth peaks in
the frequency histograms that are used for quantal analyses. A three-
dimensional analysis was done to compare the dimensions of pairs of
dendritic spines synapsing with individual axonal boutons. When the pairs
of spines associated with a single bouton arose from different dendrites,
at least some of which were likely to have come from different cells, the
differences between their volumes and the areas of the postsynaptic
densities were on average 100% and ranged up to 650%.(ABSTRACT TRUNCATED AT
400 WORDS)
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