Journal of Neuroscience, Vol 12, 1847-1858, Copyright © 1992 by Society for Neuroscience
Synapses formed by identified retinogeniculate axons during the segregation of eye input
G Campbell and CJ Shatz
Department of Neurobiology, Stanford University School of Medicine, California 94305.
The synaptic organization of identified retinogeniculate axons was studied
during the prenatal development of eye-specific layers in the LGN of the
cat. During this period, retinogeniculate axons undergo stereotyped
morphological changes. Retinogeniculate axons originating from one eye and
passing through LGN territory destined to be solely innervated by the other
eye (inappropriate territory) initially give rise to many side branches. As
the eye-specific layers emerge, these axons elaborate extensive terminal
arbors within territory appropriate to their eye of origin and concurrently
retract their side branches from inappropriate territory (Sretavan and
Shatz, 1986). These transient side branches may therefore represent a
morphological substrate for the observed functional convergence of inputs
from the two eyes onto common LGN neurons during prenatal development
(Shatz and Kirkwood, 1984). This possibility was investigated by examining
whether identified axons and their side branches form synapses in
inappropriate territory. Three retinogeniculate axons from two fetuses aged
embryonic day 53 (E53) and E57 were filled with HRP in an in vitro
preparation, prior to being processed for electron microscopy (EM). The
HRP-filled axons, originating from the contralateral eye, were first
reconstructed at the light microscope level. The portion of axon passing
through the center of ipsilaterally innervated layer A1 was then serially
sectioned and reconstructed by EM. Two sets of 450 serial EM sections
revealed that all three contralateral axons established synaptic contacts
in ipsilateral territory. Many of these synapses were made by side branches
and a few were even formed by the main axon trunks. Both side branches and
trunks formed mainly en passant asymmetrical contacts that were associated
with spherical synaptic vesicles and that were apposed to immature
dendritic elements and dendritic shafts. For comparison, a portion of the
same E53 axon within the future contralateral layer A was also serially
sectioned and reconstructed for EM. Within this contralateral zone, the E53
axon formed synaptic contacts similar to those established in the
ipsilateral region, except that in the appropriate zone they contained
significantly more synaptic vesicles. These results demonstrate that axons
from the contralateral eye can establish synapses in territory
simultaneously innervated by the ipsilateral eye, both via side branches
and by means of contacts along the main axon trunk. Thus, the development
of eye-specific layers is accompanied by the formation and subsequent
elimination of synapses that almost certainly represent a morphological
substrate for the known transient functional convergence of inputs from the
two eyes.
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