Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat

Abstract

The effects of long-term monocular visual deprivation (MD) on the structure of the terminal arborizations of individual Y-type geniculocortical axons was studied in the cat's cortical area 18. Physiologically classified axons were filled with HRP by intracellular injection, and the three-dimensional distribution of the axons' terminal arborizations was quantified. Individual boutons observed at the light microscope (LM) level were verified as sites of synaptic contact by correlated light and electron microscopy (EM). Single boutons were serially sectioned and reconstructed for subsequent three-dimensional analysis. The arborizations of 17 Y-axons [6 normal (N), 6 nondeprived (ND), and 5 deprived (D)] were analyzed at the LM level, and 372 boutons (104 N, 129 ND, and 139 D) were fully reconstructed from serial sections for analysis at the EM level. MD leads to an expansion in the size of ND arborizations and a variable reduction in the size of the D arbors, which also have a higher bouton density than ND arborizations. ND axons form ectopic synapses, contacting proportionally more dendritic shafts than N or D boutons, and form more synapses per bouton, on average, than either N or D boutons. Compared to ND and N boutons, boutons of D axons are smaller, have fewer mitochondria, generally form synapses on a single target (usually dendritic spines), and occasionally make no synaptic contacts. The structural changes in the extent of individual axon arborizations may be the basis for change in ocular dominance column size with MD. However, the higher bouton density and variable effect on the extent of D axon arborization size suggest that considerable geniculocortical innervation from the deprived eye remains intact. The change in target preference for ND axons suggests that instead of a direct competition for postsynaptic sites by the developing geniculocortical axons innervated by the two retinas, the ND axon arborizations expand to invade synaptic space not normally occupied in such high proportion in the normal cortex. The severe changes in individual boutons following MD indicate that arborization size alone is not the only structural substrate underlying the altered responses of cortical neurons; changes in synaptic distribution onto target neurons may also play a role.