Remodeling of retinal ganglion cell dendrites in the absence of action potential activity

Abstract

The dendrites of ganglion cells in the retina have an excess number of spines and branches that are normally lost during the first postnatal month of development. We investigated whether this dendritic remodeling can be prevented when the action potential activity of ganglion cells is abolished by chronic intraocular injections of tetrodotoxin (TTX) during the first 4 or 5 postnatal weeks in the cat. Dendritic tree morphologies of alpha and beta ganglion cells from TTX-treated, non-TTX-treated (contralateral eye), and normal control retinae were compared after intracellular filling with Lucifer yellow. Qualitative observations and quantitative measurements indicate that TTX treatment does not prevent the normally occurring loss of spines and dendritic branches. Indeed, the dendritic trees of both alpha and beta cells in TTX injected eyes actually have even fewer spines and branches than normal cells at equivalent ages. However, because the total dendritic lengths of these cells are also reduced after TTX blockade, spine density is indistinguishable from untreated animals at the same age. In addition, although dendritic field areas are not altered with treatment, the complexity of the dendritic trees is reduced. These observations suggest that dendritic remodeling can occur in the absence of ganglion cell action potential activity. Thus, the factors that influence the dendritic and axonal development of retinal ganglion cells must differ, because similar TTX treatment during the period of axonal remodeling does have profound effects on the final pattern of terminal arborizations.

Electrical activity regulates dendritic reorganization in ganglion cells after neonatal retinal lesion in the cat

“…Similar results have been reported in primary visual cortex, where the axonal segregation in ocular dominance columns is prevented by TTX treatment during the critical period (Stryker and Harris, 1986). But surprisingly, the blockade of electrical activity in the developing retina has little effect on the remodeling of ganglion cell dendritic arborizations, which takes place during the first month of postnatal life (Wong et al, 1991).…”

Mice Lacking Specific Nicotinic Acetylcholine Receptor Subunits Exhibit Dramatically Altered Spontaneous Activity Patterns and Reveal a Limited Role for Retinal Waves in Forming ON and OFF Circuits in the Inner Retina

“…Although a general blockade of action potentials with intraocular injections of tetrodotoxin had little effect on the dendritic structure of RGCs in both embryonic (Campbell et al, 1997) and postnatal cat retina (Wong et al, 1991), manipulations of neurotransmitter systems providing synaptic input to ganglion cells had more profound effects on RGC anatomy and function. For example, Sernagor and Grzywacz (1996) demonstrated that blockade of retinal wave activity in turtle retina with intraocular injection of the general nicotinic acetylcholine receptor (nAChR) antagonist D-tubocurarine prevented the dark-rearing-induced changes in RGC receptive fields.…”

Receptive Field Mosaics of Retinal Ganglion Cells Are Established Without Visual Experience

“…Vision is critical for the normal development of horizontal and bipolar cells (Bayley and Morgans 2007;Lee et al 2008), and there are indications that it is also needed for the normal maturation of RGC dendrites (Sernagor and Mehta 2001;Tian and Copenhagen 2003;Wingate and Thompson 1994;Wong et al 1991). However, many aspects of RGC development are immune to alterations in neural activity (Daw and Wyatt 1974;Elstrott et al 2008;Kerschensteiner et al 2009;Lau et al 1990).…”