The Developmental Remodeling of Eye‐Specific Afferents in the Ferret Dorsal Lateral Geniculate Nucleus

Speer, Colenso M.; Mikula, Shawn; Huberman, Andrew D.; Chapman, Barbara

doi:10.1002/ar.21001

Cited by 15 publications

(32 citation statements)

References 70 publications

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“…Consistent with what has been previously reported in adult enucleates (7,10), neonatal monocular enucleation resulted in an expansion of the ipsilateral projection by P10, while laminar organization was preserved (23)(24)(25) (Fig. 1 A and B; binocular saline, 0.115 ± 0.004 mm 2 ; monocular saline, 0.304 ± 0.019 mm 2 ; P < 0.0001).…”

Section: Resultssupporting

confidence: 90%

“…As predicted, the blockade of retinal waves from P1 to P10 prevented the correct lamination of the ipsilateral projection in enucleates, with no identifiable A1 or C1 lamina (23)(24)(25) found at P10 (Fig. 1A, Lower Right).…”

Section: Resultssupporting

confidence: 75%

“…1C; binocular saline, 0.550 ± 0.016; monocular saline, 0.525 ± 0.013; P = 0.626). These results demonstrate that when intereye competition is disrupted in binocular ferrets, ipsilaterally projecting afferent terminals will preferentially target the medial dLGN, which corresponds to the contralateral A lamina (23)(24)(25).…”

Section: Resultsmentioning

confidence: 61%

“…5) but not in adult mice (22,53)? One possibility is that the laminar structure of the ferret dLGN limits the extent of its developmental plasticity (23)(24)(25)54). Because ferret dLGNs have cellular lamination, unlike the mouse, and also express molecules inhibiting neurite outgrowth between laminae (55), it is likely that retinogeniculate plasticity is reduced at more mature time points.…”

Section: Discussionmentioning

confidence: 99%

“…However, studies have suggested that retinal waves might play additional roles in the development of the retinogeniculate pathway. When retinal waves are blocked during early development, mature lamination in the adult is abnormal (23)(24)(25), while eye-specific segregation recovers (26,27). These results uncovered a retinal wave-dependent window for the development of retinogeniculate lamination.…”

mentioning

confidence: 84%

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Retinal waves regulate afferent terminal targeting in the early visual pathway

Failor

Chapman

Cheng

2015

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

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Current models of retinogeniculate development have proposed that connectivity between the retina and the dorsal lateral geniculate nucleus (dLGN) is established by gradients of axon guidance molecules, to allow initial coarse connections, and by competitive Hebbianlike processes, to drive eye-specific segregation and refine retinotopy. Here we show that when intereye competition is eliminated by monocular enucleation, blocking cholinergic stage II retinal waves disrupts the intraeye competition-mediated expansion of the retinogeniculate projection and results in the permanent disorganization of its laminae. This disruption of stage II retinal waves also causes longterm impacts on receptive field size and fine-scale retinotopy in the dLGN. Our results reveal a novel role for stage II retinal waves in regulating retinogeniculate afferent terminal targeting by way of intraeye competition, allowing for correct laminar patterning and the even allocation of synaptic territory. These findings should contribute to answering questions regarding the role of neural activity in guiding the establishment of neural circuits.retinal waves | retinogeniculate | axon-axon competition | receptive fields | retinotopy T he brain employs several strategies to guide the establishment of correct neural connectivity (1, 2). It has been well recognized that the high specificity of connections between the retina and the dorsal lateral geniculate nucleus (dLGN) is established through several factors. These include gradients of axon guidance molecules that guide the initial coarse targeting of afferent terminals (3-6), and spontaneous retinal activity (retinal waves) that drives competitive processes important for the refinement and segregation of afferent terminal branches (2, 7-15).Retinal waves are spontaneous propagating bursts of correlated retinal ganglion cell (RGC) activity and have been classified into three developmental stages (1, 15). Stage II retinal waves (from here on also referred to as retinal waves) are extensively studied and have been found to be critical for the development of retinofugal pathways (1, 2, 15). They are mediated by cholinergic signaling from starburst amacrine cells onto RGCs (8,13,[16][17][18] and have been hypothesized to drive the Hebbian-like remodeling of RGC afferent terminals (19,20). Retinal waves play crucial roles in both the establishment of eye-specific segregation (8,12,14,20,21), through the removal of afferent branches from opposing putative eyespecific domains, and the refinement of afferent terminals within eye-specific laminae, which is believed to be necessary for the establishment of fine-scale retinotopy (12,22). However, studies have suggested that retinal waves might play additional roles in the development of the retinogeniculate pathway. When retinal waves are blocked during early development, mature lamination in the adult is abnormal (23-25), while eye-specific segregation recovers (26,27). These results uncovered a retinal wave-dependent window for the development of retinogen...

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Section: Resultssupporting

confidence: 90%

Section: Resultssupporting

confidence: 75%

Section: Resultsmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 84%

See 3 more Smart Citations

Retinal waves regulate afferent terminal targeting in the early visual pathway

Failor

Chapman

Cheng

2015

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

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Investigation of cytoskeleton proteins in neurons of the cat lateral geniculate nucleus

Duffy

Crowder

LeDue

2011

J of Comparative Neurology

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The gross structure of neurons is supported by proteins that compose the cytoskeleton. Neurofilaments are intermediate cytoskeletal proteins that contribute to neuron structure and function, and three neurofilament subunits different in their molecular mass assemble to form heteropolymers that produce a structure-providing intracellular scaffold. The light neurofilament subunit is obligatory and can assemble with either the medium or heavy subunit, indicating some degree of independence between subunits. The presence of the heavy subunit has been shown to be associated with mature cells and is linked to large neurons in the cerebral cortex and thalamus. Spectrin is a membrane-associated actin-binding protein that, like neurofilament, has been linked to neuron shape. In this study of the cat dorsal lateral geniculate nucleus (dLGN) we examined whether labeling for neurofilament subunits and spectrin is linked to neuron size. We found that about one-third of neurons contained a visible amount of labeling for each neurofilament subunit, and the bulk of these labeled cells were large in comparison to the general population of neurons. The distribution of neuron sizes was not different between neurofilament subunits, indicating that neurofilament subunit content is not determined by neuron size. Spectrin labeling was evident in most dLGN neurons, and was not related to the size of neurons. That reactivity for neurofilament was predominant in large cells led us to directly examine the relationship between neurofilament and interneurons. The large majority of neurofilament-positive neurons did not contain GABA, indicating that neurofilament is predominant in projection cells and not in interneurons.

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Postnatal development of chorda tympani axons in the rat nucleus of the solitary tract

Wang

Corson

Hill

et al. 2012

J of Comparative Neurology

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The chorda tympani nerve (CT), one of three nerves that convey gustatory information to nucleus of the solitary tract (NTS), displays terminal field reorganization after postnatal day 15 in the rat. Aiming to gain insight into mechanisms of this phenomenon, CT axon projection field and terminal morphology in NTS subdivisions were examined using tract tracing, light microscopy, and immuno-electron microscopy at four postnatal ages: P15, P25, P35, and adult. The CT axons that innervated NTS rostrolateral subdivision both in the adult and in P15 rats were morphologically distinct from those that innervated the rostrocentral, gustatory subdivision. In both subdivisions, CT terminals reached morphological maturity before P15. Rostrolateral, but not rostrocentral axons, went through substantial axonal branch elimination after P15. Rostrocentral CT synapses, however, redistribute onto postsynaptic targets in the following weeks. CT terminal preference for GABAergic postsynaptic targets was drastically reduced after P15. Furthermore, CT synapses became a smaller component of the total synaptic input to the rostrocentral NTS after P35. The results underlined that CT axons in rostrocentral and rostrolateral subdivisions represent two distinct populations of CT input, displaying different morphological properties and structural reorganization mechanisms during postnatal development.

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The Developmental Remodeling of Eye‐Specific Afferents in the Ferret Dorsal Lateral Geniculate Nucleus

Cited by 15 publications

References 70 publications

Retinal waves regulate afferent terminal targeting in the early visual pathway

Retinal waves regulate afferent terminal targeting in the early visual pathway

Investigation of cytoskeleton proteins in neurons of the cat lateral geniculate nucleus

Postnatal development of chorda tympani axons in the rat nucleus of the solitary tract

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