Elimination of action potentials blocks the structural development of retinogeniculate synapses

Kalil, Ronald E.; Dubin, Mark W.; Scott, Grayson; Stark, Louisa A.

doi:10.1038/323156a0

Cited by 77 publications

(40 citation statements)

References 22 publications

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“…First, similar treatments (intraocular injections of TTX) (Riccio and Matthews, 1985) apparently increase the naturally occurring losses of spines on pyramidal neurons of the visual cortex (see also Boothe, Greenough, Lund, and Wrege, 1979). More relevant to our study, the same treatment performed at the same postnatal ages is known to have profound effects on the formation of retinogeniculate synapses (Kalil, Dubin, Scott, and Stark, 1986) and on the final remodeling of retinal ganglion cell axons within the LGN. For example, recent intracellular labeling studies of retinogeniculate axons following neonatal TTX treatment by Sur, Garraghty, and Stryker (1985) show that Y-axon terminal arbors are severly shrunken, as are the LGN layers receiving input from ganglion cell axons in the treated eye (Kuppermann and Kasamatsu, 1984), a finding we have confirmed here.…”

Section: Effect Of Activity Blockade On Dendritic Remodelingmentioning

confidence: 90%

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

1991

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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.

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Section: Effect Of Activity Blockade On Dendritic Remodelingmentioning

confidence: 90%

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

1991

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“…Activity regulates growth cone responsiveness to guidance cues, enhancing netrin responsiveness and inhibiting myelin repulsion (Ming et al 2001). And, activity shapes the specificity of local connectivity of axons, for example in the selection and elimination of cortical innervation targets (Kalil et al 1986;Katz and Shatz 1996;Catalano and Shatz 1998). Data on the effect of activity on axon growth have been more controversial.…”

Section: Control Of Neuronal Responsiveness To Trophic Peptidesmentioning

confidence: 99%

How does an axon grow?

Goldberg¹

2003

Genes Dev.

204

138

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How do axons grow during development, and why do they fail to regrow when injured? In the complicated mesh of our nervous system, the axon is the information superhighway, carrying all of the data we use to sense our environment and carry out behaviors. To wire up our nervous system properly, neurons must elongate their axons during development to reach their targets. This is no simple task, however. The complex morphology of axons and dendrites puts neurons among the most intricate and beautiful cells in the body. Knowledge of how neurons extend axons and dendrites, elongate at a particular rate, and stop growing at the proper time is critical to understanding the development of our nervous system, yet the regulation of these processes is poorly understood. Considerable attention in recent years has focused on understanding how growth cones are guided and steered through complicated pathways (for review, see Schmidt and Hall 1998;Mueller 1999), and even how neurons initiate new processes (for review, see Da Silva and Dotti 2002), but what mechanisms are involved in elongation itself? Are environmental signals needed to drive axon growth and, if so, what are the intracellular molecular mechanisms by which they induce elongation? What controls the rate of axon growth? How do CNS neurons know whether to extend axons or dendrites? Is the signaling of axon versus dendrite growth attributable to different extracellular signals, different neuronal states, or both? All of these questions bear critically on our understanding of axon growth and here I review recent answers and approaches to the above questions, and highlight their relevance during development, injury, and disease.

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“…However, observations on congenitally anophthalmic mice suggest the tThe late appearance and slow maturation of thalamic synaptic glomeruli seem to be common phenomena. In the hamster LGd (23) and rat VB (34), glial-encapsulated glomeruli do not appear until the second postnatal week and do not take mature forms until the third postnatal week, while in the cat LGd, glomeruli do not appear until 25 days postnatally and do not mature until 40-45 days postnatally (35,36).…”

Section: Resultsmentioning

confidence: 99%

Target-controlled differentiation of axon terminals and synaptic organization.

Campbell

Frost

1987

Proc. Natl. Acad. Sci. U.S.A.

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These experiments investigate the processes regulating the morphological differentiation of synaptic connections. Electron microscopy showed that the terminal boutons and synaptic complexes of retinal afferent axons in the main thalamic visual nucleus, the dorsal lateral geniculate nucleus, differ in their morphology from those of ascending afferent axons in the main thalamic somatosensory (ventrobasal) nucleus. Developing retinal ganglion cell axons in hamsters were made to project permanently to the ventrobasal nucleus, rather than to the lateral geniculate nucleus. With respect to most of the ultrastructural features examined, the terminals and synaptic complexes of mature, anterogradely labeled retino-ventrobasal axons more closely resembled those of normal somatosensory afferents to the ventrobasal nucleus than they did those of normal retinofugal axons within the lateral geniculate nucleus. These results suggest that the ultrastructural differentiation of axon terminals and synaptic complexes is regulated largely by the target environment, although some features appear to be intrinsic to the afferent axons themselves.It is increasingly evident that patterns of axonal projection and the morphology and biochemistry of synaptic connections in the vertebrate central nervous system are determined by trophic interactions between presynaptic neurons and their targets, but the extent and details of these important processes are not well understood (1-3). A variety of observations suggest the role of postsynaptic neurons or their immediate environment (e.g., glia, extracellular matrix) in the morphological differentiation of presynaptic elements during normal development (4). For example, mossy fibers originating from widely scattered parts of the central nervous system all have the same structural type of terminal that synapses in a stereotyped way with the dendrites of cerebellar granule cells (4, 5). Furthermore, both mossy and climbing fibers, which originate from different neuronal populations, contact multiple cerebellar cell types. Both fiber types make terminals with morphologies that are unique to each of their targets, and both fiber types make the same kind of terminal when synapsing on the same cell type (5-7). Though retinal ganglion cell (RGC) axons projecting to the primary visual nucleus of the thalamus, the dorsal lateral geniculate nucleus (LGd), are collaterals of RGC axons projecting to the superior colliculus (SC) (8), the morphologies of RGC axon terminals differ in the LGd and SC (refs. 9-12; G.C., unpublished data). Similarly, auditory nerve fibers have multiple collaterals, each of which projects to a different division of the cochlear nucleus and each of which has a distinct terminal morphology (13-15).Axon terminals frequently participate in synaptic complexes called "glomeruli"-regions containing numerous neuronal elements engaged in multiple synaptic contacts and isolated from areas of simpler neuropil by sheets of astrocyte cytoplasm. Despite the preceding data from normal anim...

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Elimination of action potentials blocks the structural development of retinogeniculate synapses

Cited by 77 publications

References 22 publications

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

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

How does an axon grow?

Target-controlled differentiation of axon terminals and synaptic organization.

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