Loss of Binocular Responses and Reduced Retinal Convergence During the Period of Retinogeniculate Axon Segregation

Abstract

In the developing mammalian visual system, axon terminals from the two eyes overlap in the dorsal lateral geniculate nucleus (LGN) but then undergo a period of refinement and segregate to form distinct eye-specific domains. We report on the changes in synaptic transmission that occur in rodent LGN during the period of retinogeniculate axon segregation by using anterograde labeling techniques in conjunction with an in vitro preparation where large segments of each optic nerve are preserved. Anterograde labeling of retinal projections in early postnatal day (P) rats with cholera toxin beta subunit indicated an age-related recession in uncrossed retinal projections. Between P2 and P5 uncrossed projections occupied as much as 50% of the LGN and overlapped substantially with crossed projections. Between the first and second postnatal week uncrossed projections receded, so by P14 they assumed an adultlike profile occupying 15-20% of LGN and showed little or no overlap with crossed projections. The postsynaptic responses of LGN cells evoked by the separate stimulation of each optic nerve indicated that before P14, many relay cells were binocularly innervated and received at least four to six inputs from each eye. However, these features of retinogeniculate connectivity were transient and their attrition occurred in concert with a retraction of retinal arbors into nonoverlapping, eye-specific regions. By P18 cells were monocularly innervated and received input from one to three retinal ganglion cells. These results provide a better understanding of the underlying changes in synaptic circuitry that occur during the anatomical segregation of retinal inputs into eye-specific territories.