Spontaneous bursting and long-lived local correlation in normal and denervated tectum of goldfish

The formation of fine retinotopic order by growing optic fibers in the goldfish is thought to be mediated by the correlated firing of optic fibers from neighboring retinal ganglion cells. Although the activity of the tectal cells must also be important for this activity-dependent refinement, few studies have analyzed the pattern and local correlation of the intrinsic activity of tectal neurons and the effect of denervation on this activity. To address this issue, spontaneous (nonoptic driven) activity was analyzed and cross-correlograms were computed between individual tectal neurons using single and double electrode extracellular recordings. Recordings were made in normally innervated tectum in which the contribution of optic activity was eliminated by short-term intraocular blockade with tetrodotoxin and in denervated tecta in which the optic nerve had been severed several weeks prior. Several observations were relevant to activity-dependent refinement: First, coupling between neighboring tectal cells is weak. Second, the time duration for local correlation is relatively long, as long as 200 ms. Third, tectal neurons exhibit spontaneous bursting. Fourth, denervation increased the level of spontaneous activity in the tectum. The increased spontaneous activity and bursting following denervation implies that tectal neurons are more excitable when optic fibers are beginning to reinnervate the tectum. This could make it possible for optic fibers to drive tectal neurons at a time when their input to individual neurons is severely weakened by a lack of spatial convergence. The weak coupling between tectal cells and the consequent long-time constant for correlated activity implies a constraint on the duration of correlated retinal activity that is used for activity-dependent refinement. Since optic fibers likely need to detect the postsynaptic activity of a local group of tectal neurons, rather than that of a single neuron, the long tectal time constant means that retinal activity need not be correlated with precision much better than 200 ms because the postsynaptic circuitry cannot generate shorter correlations.