Conduction and synaptic transmission in the optic nerve and the superior colliculus during development of the retinocollicular projection in the wallaby (Macropus eugenii)

Abstract

When do the developing connections between mammalian retinal ganglion cells and the superior colliculus become functional? Evoked potentials elicited by optic nerve stimulation in the pouch young of the wallaby were used to answer the question. Up to 42 days after birth, the evoked potentials in the colliculus appeared to be generated by axon conduction. Synaptic activity was first recorded from the rostral colliculus at 45 days, and was found to be progressively more caudal, spreading to cover the colliculus, by 65 days. From the earliest indication of synaptic activity until eye opening at 140 days, current source density (CSD) analysis consistently showed the same basic pattern: an initial deep sink from synaptic activity of fast (Y type) fibres, and a more superficial longer-latency sink from slower (W type) fibres. All features became more clearly delineated with age. The indirect retinocorticocollicular connection appeared between 134 days and 146 days. The ability of optic nerve fibres to sustain action potentials precedes their formation of functional synapses with collicular neurons, which happens abruptly at three months before eye opening. CSD analysis showed that the relationship between the conduction velocity of optic nerve fibres and their depth of termination is evident from the first signs of synapse formation.

Retinotopic order in the optic nerve and superior colliculus during development of the retinocollicular projection in the wallaby ( Macropus eugenii )

“…The first stage in the wallaby, where axons were coarsely retinotopically ordered with no sign of terminal arbors and no functional connections with collicular cells (Freeman et al 1997), is not seen in fishes and frogs. In these species the projection is topographically organized and functional from the outset Gaze et al 1974;Holt and Harris 1983;Holt 1984;Sakaguchi and Murphey 1985;O'Rourke and Fraser 1986;Fujisawa 1987;Stuermer 1988;Stuermer and Raymond 1989;Kaethner and Stuermer 1992).…”

“…It appears that the formation of arbors is initiated without there having been functional connections between retinal and tectal cells (Mark et al 1993a;Freeman et al 1997). Interestingly, blockade of NMDA receptors in the rat SC during development of the retinotopic map, presumably resulting in blockade of NMDAmediated postsynaptic activity, did not prevent the formation of correctly positioned arbors but did prevent the removal of aberrant ones (Simon et al 1992).…”

GAP-43 Immunoreactivity in the brain of the developing and adult wallaby ( Macropus eugenii )

“…Beginning at about P40 and extending to P55, there is formation of retinotopically appropriate terminal zones and this phase also coincides with changes in the visual evoked potential recorded from the superior colliculus. Up to P42, evoked potentials appear to be generated solely by axon conduction, but from P45 synaptic activity can be recorded, beginning at the rostral pole and progressively spreading caudally to cover the superior colliculus by P65 (Freeman et al 1997).…”

“…Our research group has undertaken extensive studies of the structural and functional development of central sensory and cortical commissural pathways in an Australian diprotodontid metatherian, (the tammar wallaby, Macropus eugenii) (e.g. Ashwell et al 1966a;Freeman et al 1997;Marotte et al 1997;Leamey et al 1998). The aims of the present study were: firstly, to compare the spatiotemporal pattern of GAP-43 development in specific areas of the wallaby brain (e.g.…”

Spatiotemporal patterns of ontogenetic expression of parvalbumin in the superior colliculi of rats and rabbits

“…Indeed, the arrivals of the two principal (topographically organized) inputs to these layers from the contralateral and to a lesser extent ipsilateral retinae and from the ipsilateral visual cortices (for recent reviews, see Rhoades et al, 1991;Stein and Meredith, 1991;Sefton and Dreher, 1995) are in all mammals studied thus far are clearly separated in time (for review, see Robinson and Dreher, 1990;Freeman et al, 1997).…”