Early lesions of superior colliculus: factors affecting the formation of abnormal retinal projections.

Abstract

The longest fibers of the main optic tract reach the upper layers of the superior colliculus (SC) of the midbrain. Destruction of this terminal area in newborn hamsters caused striking anomalies in the distribution of the optic tract, studied after the animals were fully grown. Evidence of termination was found in areas normally devoid of such termination: in the remaining tissue of the colliculus and in the thalamic nucleus lateralis posterior (LP). An abnormally high density of termination was found in part of the ventral nucleus of the lateral geniculate body. These thalamic regions normally receive connections from SC. Retinofugal axons could also be induced to terminate in the medial geniculate body of the thalamus if the brachium of the inferior colliculus, which normally carries auditory information to this cell group, was ablated at birth together with the lesion of SC.If the superficial layers of SC were destroyed unilaterally at birth, axons from the eye contralateral to the lesion not only reached the area of early damage, but also formed an abnormal decussation, crossing the tectal midline to terminate in the medial zone of the undamaged colliculus. Axons from the two eyes <i>competed for terminal space </i>in this intact colliculus, for they terminated in a nonoverlapping manner, and if the axons from the eye contralateral to the remaining SC were eliminated at birth, the anomalously recrossing axons increased in quantity and spread across the entire SC on the 'wrong' side of the midbrain. Hamsters with such an anomaly showed wrong-direction turning in response to visual stimuli in a large part of the visual field.The less the amount of termination found in SC, the greater was the amount in LP. Thus, optic tract axons showed a <i>'pruning effect' </i>which may be attributed to a tendency for axons to conserve the quantity of their terminal arborizations. The pruning effect alone may account for the hypertrophy we found, after early SC lesions, of the dorsal terminal nucleus of the accessory optic tract. The tendency to invade vacated terminal space may be sufficient to account for an effect of early unilateral eye removal, namely, a pronounced increase in an ipsilateral retinal projection to the medial terminal nucleus of the accessory optic tract.The greatest alterations in axonal projections were seen when the two effects, competition and pruning, seemed to act jointly. Additional factors may have to be considered in fully explaining such neuroplasticity; some of these have been suggested.