Normal postnatal development of retinogeniculate axons and terminals and identification of inappropriately-located transient synapses: Electron microscope studies of horseradish peroxidase-labelled retinal axons in the hamster

Abstract

Axons from the eyes reach the dorsal lateral geniculate nucleus of the hamster at birth and both crossed and uncrossed axons spread throughout the nucleus within which they overlap extensively between postnatal days 2-6, before segregating to terminate in different parts of the nucleus by days 8-10 [So, Schneider and Frost (1978) Brain Res. 142, 343-352]. We have labelled retinal axons and their terminations between the day of birth (day 0) and day 6 by injecting one eye with horseradish peroxidase a few hours prior to sacrifice. Labelled profiles were then systematically sought, identified and their position determined, by electron microscope study of large frontal thin sections of both dorsal lateral geniculate nuclei. Labelled cross and a few labelled uncrossed axons were present at day 0 and became progressively more common over the following few days; appropriately-located labeled uncrossed axons and terminals in the centromedial part of the nucleus (future ipsilateral sector) were relatively less common than labelled crossed axons in the ventrolateral part of the nucleus (part of the future contralateral sector), particularly between days 0 and 3. Synaptic contacts established by such labelled axons were characterized by predominantly electron-lucent spherical presynaptic vesicles and a prominent postsynaptic density. At day 4, labelled uncrossed axons made synaptic contact in the future contralateral sector (which is devoid of uncrossed input after days 8-10) and a few crossed axons made synaptic contacts in the future ipsilateral sector (devoid of crossed input after days 8-10). Such terminals and their synaptic contacts, were identical to appropriately-located ones in the same material. Inappropriately-located terminals were not found in the future contralateral sector at day 6, or in adults. No specialized contacts were observed between inappropriately-located axons or terminals and either other axon terminals or glial cell processes. Thus, during the development of the hamster retinogeniculate projection, inappropriately-located axons establish transient synaptic contacts with geniculate cells, and these contacts are lost as the segregated adult pattern of projections is established. The way in which inappropriately-located synaptic contacts are eliminated, and the factors responsible for their disappearance are still uncertain, but the well-differentiated fine structure of the transient synaptic specializations and evidence from physiological studies of the developing retinogeniculate projections in the cat [Shatz and Kirkwood (1984) J. Neurosci., 4, 1378-1397] and of the developing peripheral nervous system [Purves and Lichtman (1980) Science, N.Y. 210, 153-157], suggest that these transient synapses are functional.