Metabolic changes accompanying denervation and reinnervation of the dentate gyrus of the rat measured by [ 3H]2-deoxyglucose autoradiography

Abstract

The pattern of 2-deoxyglucose (2-DG) utilization was quantitatively analyzed in the dentate gyrus of the rat 1, 2, 4, 6, 8, 10, 12, 14, and 26 to 28 days after unilateral destruction of the entorhinal cortex through the use of a [ 3H]2-DG autoradiographic procedure. Grain counts were taken in the portion of the neuropil denervated by the lesion (the outer stratum moleculare), in nondenervated portions of the neuropil where normal innervation survives (the inner stratum moleculare), and over the lamina occupied by granule cell somata (stratum granulosum). Unilateral lesions of the entorhinal area resulted in rather slight (5 to 10%) decreases in 2-DG utilization in the denervated dentate gyrus compared with a comparable region on the contralateral (control) side between 1 to 4 days postlesion. These decreases were not restricted to the denervated portions of the neuropil, but rather appeared throughout the zones occupied by the postsynaptic cells. Between 6 and 10 days postlesion, however, there was a dramatic increase in 2-DG uptake in the outer stratum moleculare, whereas uptake in the inner stratum moleculare and stratum granulosum was as low or lower than during the early postlesion period. After 12 days postlesion, 2-DG uptake in the outer stratum moleculare again decreased, such that all laminae exhibited uptake which was slightly lower (10 to 15% compared with the contralateral control) than during the early postlesion period. Because the decreases in 2-DG uptake were observed throughout the territory occupied by the postsynaptic cell and were not restricted to the denervated laminae, we conclude that the denervation resulted in general decreased metabolism throughout the postsynaptic cell. Because the increases in 2-DG utilization at 6 to 10 days postlesion occurred during the time at which synaptic proliferation (sprouting) would be occurring, we suggest that this increased 2-DG utilization may reflect increased metabolic activity in afferent or postsynaptic elements during lesion-induced synaptogenesis.