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Journal of Neuroscience, Vol 6, 1021-1036, Copyright © 1986 by Society for Neuroscience
A role for action-potential activity in the development of neuronal connections in the kitten retinogeniculate pathway
MW Dubin, LA Stark and SM Archer
The role of action potentials in the development of proper synaptic
connections in the mammalian CNS was studied in the kitten retinogeniculate
pathway. Our basic finding is that there is improper segregation of retinal
inputs onto LGN cells after prolonged retinal action-potential blockade.
Retinal ganglion cell firing was silenced from birth by repeated monocular
injections of TTX. The resulting ganglion cell connections in the LGN were
studied electrophysiologically after the action-potential blockade was
ended. Most cells in the deprived LGN layers received excitatory input from
both ON-center and OFF-center type ganglion cells, whereas LGN cells
normally receive inputs only from ON-center or OFF-center ganglion cells,
but not from both types. Improper segregation of ON and OFF inputs has
never been reported after other types of visual deprivation that do not
block ganglion cell activity. Control experiments showed that receptive
fields in the nondeprived LGN layers were normal, that ganglion cell
responses remained normal, and that there was no obvious ganglion cell
loss. We also showed that individual LGN cells with ON and OFF excitatory
inputs were not present in normal neonatal kittens. Two other types of
improper input segregation in response to action- potential blockade were
also found in the deprived LGN layers. (1) A greater than normal number of
LGN cells received both X- and Y-type ganglion cell input. (2) Almost half
of the cells at LGN layer borders were excited binocularly. Recovery of LGN
normality was rapid and complete after blockade that lasted for only 3
weeks from birth, but little recovery was seen after about 11 weeks of
blockade. The susceptibility to action-potential blockade decreased during
the first 3 postnatal weeks. These findings may result from axon-terminal
sprouting or from the failure of axon terminals to retract. The results are
consistent with the idea that normally synchronous activity of neighboring
ganglion cells of like center-type may be used in the refinement of
retinogeniculate synaptic connections.
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