The morphological sequelae induced by target removal were studied on a
dult cat abducens internuclear neurons at both the somata and terminal
axon arborization levels. The neuronal target-the medial rectus moton
eurons of the oculomotor nucleus-was selectively destroyed by the inje
ction of toxic ricin into the medial rectus muscle. Retrograde labelin
g with horseradish peroxidase demonstrated the survival of the entire
population of abducens internuclear neurons up to one year after targe
t removal. However, soma size was reduced by about 20% three months po
stlesion and maintained for one year. At the ultrastructural level, a
considerable deafferentation of abducens internuclear neurons was obse
rved at short intervals (i.e. 10 days after lesion). Large regions of
the plasmalemma appeared devoid of presynaptic boutons but were covere
d instead by glial processes. The detachment of synaptic endings was s
elective on abducens internuclear neurons since nearby motoneurons alw
ays showed a normal synaptic coverage. By one month, abducens internuc
lear neurons recovered a normal density of receiving axosomatic synaps
es. Anterogradely biocytin-labeled axon terminals of abducens internuc
lear neurons remained in place after the lesion of medial rectus moton
eurons, although with a progressive decrease in density. Ultrastructur
al examination of the oculomotor nucleus 10 days after the lesion reve
aled numerous empty spaces left by the dead motoneurons. Targetless bo
utons were observed surrounded by large extracellular gaps, still appo
sed to remnants of the postsynaptic membrane or, finally, ensheathed b
y glial processes. At longer intervals (>one month), the ultrastructur
e of the oculomotor nucleus was re-established and labeled boutons wer
e observed contacting either unidentified dendrites within the neuropi
l or the soma and proximal dendrites of the oculomotor internuclear ne
urons that project to the abducens nucleus. Labeled boutons were never
found contacting with the oculomotor internuclear neurons either in c
ontrol tissue or at short periods after ricin injection. These results
indicate that the availability of undamaged neurons close to the lost
target motoneurons might support the long-term survival of abducens i
nternuclear neurons. Specifically, the oculomotor internuclear neurons
, which likely suffer a partial deafferentation after medial rectus mo
toneuron loss, constitute a potential new target for the abducens inte
rnuclear neurons. The reinnervation of a new target might explain the
recovery of synaptic and firing properties of abducens internuclear ne
urons after medial rectus motoneuron lesion, which occurred with a sim
ilar time course, as described in the accompanying paper [de la Cruz R
. R. et al. (1994) Neuroscience 58, 81-97.]