Synapses formed by identified retinogeniculate axons during the segregation of eye input

Abstract

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.

The Developing Synapse: Construction and Modulation of Synaptic Structures and Circuits

“…Visualization of synaptic vesicle distribution along axon arbors in fixed tissues showed punctate synaptic protein localization along the entire extent of the arbor (20,21), suggesting that synapses are evenly distributed along the axon arbor. Electron microscopy studies also revealed that ul-trastructurally identified synapses are localized throughout the axon arbor (22,23), an observation recently confirmed by in vivo imaging studies (8). In more mature arbors, however, ultrastructurally identified synapses are preferentially localized to distal end branches (23).…”

Developmental changes in electrophysiological properties of LGNd neurons during reorganization of retinogeniculate connections

“…Another important factor may be the depolarized levels of the resting membrane potential at early postnatal ages, which may contribute to an increased duration of excitatory postsynaptic potentials at the immature retinogeniculate synapse (Ramoa and McCormick, 1994). Enhanced excitatory transmission may be especially important at a time when synapses probably release fewer quanta of neurotransmitter per action potential than in the adult (Campbell and Shatz, 1992).…”

Mechanisms Underlying Development of Visual Maps and Receptive Fields

“…In mice and ferrets, eyespecific retinogeniculate segregation occurs during the first ten days of postnatal life (P1-10) (Godement et al 1984,Jaubert-Miazza et al 2005 (Figure 1). Individual-axon labeling studies indicate that eyespecific segregation reflects two general processes: (a) synapse and axon arbor elaboration and (b) synapse and axon arbor elimination (Campbell & Shatz 1992;Sretavan & Shatz 1984, 1987. Electrophysiological recordings indicate that before segregation, RGC axons from both eyes can drive activity in individual LGN neurons.…”