Journal of Neuroscience, Vol 11, 2920-2930, Copyright © 1991 by Society for Neuroscience
The remodeling of synaptic extracellular matrix and its dynamic relationship with nerve terminals at living frog neuromuscular junctions
LL Chen, DB Folsom and CP Ko
Department of Biological Sciences, University of Southern California, Los Angeles 90089-2520.
The question of whether the synaptic extracellular matrix undergoes
remodeling and how this remodeling is related to nerve terminal plasticity
was examined in living neuromuscular junctions of adult frogs. Sartorius
muscles were double stained with a fluorescent nerve terminal dye
4-(4-diethylamino-styryl)-N-methylpyridinium iodide (4-Di- 2-Asp) and
rhodamine-tagged peanut agglutinin (PNA) which recognizes synaptic
extracellular matrix. Both nerve terminals and synaptic extracellular
matrix in 200 identified normal junctions were visualized in vivo two or
three times over a period of 2.6-6 months. The majority of neuromuscular
junctions (NMJs) showed remodeling of both nerve terminals and synaptic
extracellular matrix. Only 2.5% showed no changes in either synaptic
element. The most commonly seen remodeling involved correlated changes in
both nerve terminals and synaptic extracellular matrix. In this large
group, while some junctions (20%) showed overall proportionate changes in
all branches, most junctions (68%) showed disproportionate extension and/or
retraction of some but not all individual branches. Another group of NMJs
(9.5%) showed mismatched changes in the nerve terminal and synaptic
extracellular matrix. In this group, some NMJs showed a decrease in the
nerve terminal length without a corresponding reduction in synaptic
extracellular matrix length. In other junctions that displayed extension of
branches, the PNA-stained matrix was longer than the distal tip of the
nerve terminal. Morphometric analysis indicated an average increase of
15.6% in total nerve terminal length and 13.6% in total synaptic
extracellular matrix length. Although almost all NMJs displayed remodeling
in at least one branch, about 50% of the 2201 individual branches examined
did not show changes. The average change was 8.9% growth in the length of
individual nerve terminal branches and 8.3% growth in the length of
individual branches of synaptic extracellular matrix. There was no
significant difference in the morphometry between the repeatedly observed
junctions and the previously unobserved control junctions. Furthermore,
junctions in which the synaptic extracellular matrix was longer than the
nerve terminal also were seen in control as well as in experimental
muscles. Cases where the nerve terminals were longer than the synaptic
extracellular matrix were never observed in newly arising junctional
branches. The present study has shown extensive remodeling in not only the
nerve terminal but also the synaptic extracellular matrix in adult living
frog NMJs. Results suggest that nerve terminals retract before the synaptic
extracellular matrix. A hypothesis that extension of synaptic extracellular
matrix precedes nerve terminal growth during synaptic remodeling is
proposed.
Previous Article | Next Article
