Recovery of the ipsilateral oculotectal projection following nerve crush in the frog: Evidence that retinal afferents make synapses at abnormal tectal locations

Abstract

The ipsilateral oculotectal projection in the frog is a topographic mapping of the binocular part of the visual field of one eye on the ipsilateral tectal lobe. The underlying neuronal circuitry consists of the topographic, crossed retinotectal projection and an intertectal pathway which relays information from a given point in one tectal lobe to the visually corresponding point in the other. During optic nerve regeneration, there is a period when the terminals of retinotectal afferents are found at abnormal locations in the opposite tectal lobe. Whether they form functional synapses at this time is not known. If so, one would expect to observe correlated abnormalities in the ipsilateral oculotectal projection. To determine whether such abnormalities exist, we have made parallel electrophysiological studies of the recovery of the retinotectal and ipsilateral oculotectal projections following crush of one optic nerve. The earliest stage of recovery was characterized by lack of significant topographic order in the retinotectal projection and by the absence of a physiologically observable ipsilateral projection. Within a short time, the retinotectal projection became topographically organized and a similarly organized ipsilateral projection appeared. While topographic, the retinotectal projection at intermediate times was abnormal in that the multiunit receptive fields recorded at individual tectal loci were greatly enlarged. Multiunit receptive fields were similarly enlarged in the ipsilateral projection. In addition, some ipsilateral fields included areas of visual space not normally represented in the projection. The abnormalities in both projections subsequently disappeared over the same time course. Throughout recovery there was a high correlation between multiunit receptive field sizes in the contralateral tectal lobe and those at visually corresponding points in the ipsilateral tectal lobe. Enlarged multiunit receptive fields in the contralateral tectal lobe could not be accounted for in terms of optical or retinal abnormalities since single unit receptive field sizes were normal. Nor could they be accounted for in terms in changes in recording characteristics since simultaneously recorded fields activated by the undisturbed eye were normally sized. We conclude that the enlarged fields in the contralateral tectal lobe indicate the presence at individual tectal loci of afferents from wider than normal retinal regions. Similar considerations ruled out optical, retinal, and recording abnormalities as the explanation for the enlarged multiunit receptive fields in the ipsilateral tectal lobe. The enlarged ipsilateral multiunit receptive fields were recorded only at tectal loci normally involved in the ipsilateral projection and were locally abolished by local lesions in the opposite tectal lobe. These and other observations mentioned make it unlikely that the enlarged ipsilateral multiunit receptive fields result from abnormalities in the intertectal relay itself. Single unit receptive field sizes in the ipsilateral projection were enlarged, as would be expected if there was abnormally wide functional convergence onto elements of the intertectal relay. We conclude that during the recovery of the ipsilateral projection there are abnormalities of the kind expected if retinal terminals for functional synapses at abnormal locations in the contralateral tectal lobe.