Compensatory and transneuronal plasticity after early collicular ablation

Abstract

Plasticity within the visual system was assessed in the quokka wallaby following unilateral superior collicular (SC) ablation at postnatal days (P) 8-10, prior to the arrival of retinal ganglion cell (RGC) axons. At maturity (P100), projections were traced from the eye opposite the ablation, and total RGC numbers were estimated for both eyes. Ablations were partial (28-89% of SC remaining) or complete (0-5% of SC remaining). Projections to the visual centers showed significant bilateral (P < 0.05) increases in absolute volume. Minor anomalous projections also formed within the deep, surviving non-retino-recipient layers of the ablated SC and via a small bundle of RGC axons recrossing the midline to innervate discrete patches in the SC contralateral to the lesion. Total absolute volume of projections did not differ between partial and complete ablations; moreover, values did not differ from normal (P > 0.05). Compared with normal, total RGC numbers were significantly (P < 0.05) reduced in the eye opposite the ablation but increased (P < 0.05) in the other eye. Consequently, the sum of the two RGC populations did not differ from normal (P > 0.05). As in rodents, the visual system in quokka compensates following injury by maintaining a set volume of arborization but does so by forming only minor anomalous projections. Furthermore, increased RGC numbers in the eye ipsilateral to the lesion indicate that compensation occurs transneuronally, thus maintaining total numbers of projecting neurons. The implication is that the visual system acts in concert following unilateral injury to maintain set values for RGC terminal arbors as well as their cell bodies.