Metabolic changes in the superior colliculus after retinal receptor loss—Neurotrophic interactions in the inactive visual system

Abstract

In the mature rat, direct denervation by means of eye enucleation resulted in a temporary metabolic depression followed by “recovery” in primary visual centers as determined by the 2-deoxyglucose technique (4). After unilateral destruction of the retinal receptor layer by means of intense light, the superior colliculus (SC) demonstrated this same depression-recovery process. Because receptor destruction is believed to silence ongoing ganglion cell activity, and because the SC changes occurred whether or not ganglion cells sustained damage, it appeared that direct denervation of colliculus neurons was not necessary to initiate the depression-recovery sequence and that lack of activity or “disuse” was the critical factor. The silencing effect of the receptor destruction was confirmed when tetrodotoxin (TTX) injections into the damaged eye 2 months after damaging light exposure only slightly affected metabolic activity in the recovered colliculus. Binocular TTX injections in unilaterally light-damaged rats after 2 months of recovery resulted in greater depression in the normal colliculus than in the “recovered” colliculus, again suggesting that increases in glucose metabolism over time reflected physiological adjustments in the SC to loss of afferent activity. The strong depression in the SC fed by the normal eye after TTX injection confirmed that tonic retinal afferent activity was important to the metabolic integrity of the SC and that cessation of such activity could lead at least to depression in the system. In a final group of 2-month recovery animals the light-damaged eye was enucleated. Presumably, if withdrawal of afferent activity is solely responsible for initiating the depression-recovery sequence, the destruction of already silenced retinal ganglion cells would have no effect on the recovered SC. This was not found to be the case. In fact, enucleation reinstated the metabolic depression in the recovered SC and demonstrated that denervation per se resulted in depression of glucose metabolism in postsynaptic neurons. Even in the absence of impulse activity, visual system neurons maintained trophic interactions.