Role of the target in directing the outgrowth of retinal axons: Transplants reveal surface‐related and surface‐Independent cues

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Abstract
In the present investigation we have examined whether retinal axons can be directed to the superior colliculus via an alternate route when they do not have access to their normal substrates along the optic tract. To address this issue we transplanted embryonic mouse retinae into the mid-brain parenchyma and to various positions around the outer surface of the midbrain of newborn rats and then examined the development of projections from the transplanted tissue. The projections from cortical grafts placed in the midbrain were studied to determine whether axons from different classes of neurons respond to the same cues for outgrowth. When retinae were placed within the midbrain close to the cerebral aqueduct, axons projected dorsally to the superficial layers of the superior colliculus. Directed outgrowth was seen from the earliest time a projection could be detected and was independent of whether the superior colliculus still received host optic afferents. In contrast, the major projection from similarly placed cortical transplants was directed toward the ventral part of the midbrain. Deafferentation of midbrain corticorecipient areas did not affect the projection patterns from either type of graft. Projections from retinae placed more ventrally in the midbrain tegmentum could not be detected. However, retinae placed on the surface of the midbrain, even as far ventral as the cerebral peduncle at the level of the inferior colliculus, always had a projection to the superior colliculus that ran along the brain-stem surface. These observations, suggest that the superior colliculus exerts a positive influence on the growth of optic axons to the midbrain. However, while target cues appear to be able to support retinal axon growth through the midbrain parenchyma, their range appears to be limited, and at distances beyond the extent of their influence, optic fiber outgrowth occurs only over the surface of the brain. It is suggested, therefore, that there are both local surface-related and target-derived surface-independent cues that guide optic axons to the tectum in developing mammals.