Spontaneous regeneration of severed optic axons restores mapped visual responses to the adult rat superior colliculus

Abstract

To test whether a spontaneous and functional regeneration of severed axons could occur within the adult mammalian central nervous system, a long-term recovery of microelectrode-mapped visual response was sought in the superior colliculus (SC) after its total or near-total abolition by a precise guillotine cut of the retinocollicular pathway. Recoveries were found 3 weeks or later in 15 of the 36 animals studied; in 10 of these recoveries, half or more of the width of the SC was involved. The recovered responses were often activated from within a normally small area of the visual field. Appropriate retinotopic maps were restored. Intraocular horseradish peroxidase tracing revealed a variety of novel optic trajectories, passing around lesions even of totally cut pathways, which eventually terminated in normally retinorecipient layers of those recovered SCs. Such detours could not be explained by a mechanical reorientation of brain structures. When exactly comparable lesions were examined within a few days, there were no detours: severed optic axons faced the cuts. In long-term animals where responsiveness remained absent, optic axonal reorientations were observed near lesions but the SC was not innervated. Extensive long-term recoveries were in marked contrast to the occasional rapid ones, found within a few days postlesion, which involved only an outermost silenced border of SC. These were attributed to a rapid reversal of conduction failure in spared, bordering, axons of this topographically organized pathway. The findings support the conclusion that, after they are cut, numbers of optic axons can regenerate to the SC and restore appropriate circuitry therein.