Retinal waves regulate afferent terminal targeting in the early visual pathway

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 Hebbian-like 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 long-term 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.

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The role of retinal waves and synaptic normalization in retinogeniculate development

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1999.0400 ◽

1999 ◽

Vol 354 (1382) ◽

pp. 497-506 ◽

Cited By ~ 19

Author(s):

Stephen J. Eglen

Keyword(s):

Normal Development ◽

Ocular Dominance ◽

Visual Space ◽

Prenatal Development ◽

Dorsal Lateral Geniculate Nucleus ◽

Retinal Waves ◽

Retinal Activity ◽

Dorsal Lateral Geniculate ◽

Activity Dependent

The prenatal development of the cat retinogeniculate pathway is thought to involve activity–dependent mechanisms driven by spontaneous waves of retinal activity. The role of these waves upon the segregation of the dorsal lateral geniculate nucleus (LGN) into two eye–specific layers and the development of retinotopic mappings have previously been investigated in a computer model. Using this model, we examine three aspects of retinogeniculate development. First, the mapping of visual space across the whole network into projection columns is shown to be similar to the mapping found in the cat. Second, the simplicity of the model allows us to explore how different forms of synaptic normalization affect development. In comparison to most previous models of ocular dominance, we find that subtractive postsynaptic normalization is redundant and divisive presynaptic normalization is sufficient for normal development. Third, the model predicts that the more often one eye generates waves relative to the other eye, the more LGN units will monocularly respond to the more active eye. In the limit when one eye does not generate any waves, that eye totally disconnects from the LGN allowing the non–deprived eye to innervate all of the LGN. Thus, as well as accounting for normal retinogeniculate development, the model also predicts development under abnormal conditions which can be experimentally tested.

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Role of GABAergic inhibition in shaping the spatial frequency tuning of neurons and its contrast dependency in the dorsal lateral geniculate nucleus of cat

European Journal of Neuroscience ◽

10.1111/ejn.12149 ◽

2013 ◽

Vol 37 (8) ◽

pp. 1270-1283 ◽

Cited By ~ 3

Author(s):

Akihiro Kimura ◽

Satoshi Shimegi ◽

Shin'ichiro Hara ◽

Masahiro Okamoto ◽

Hiromichi Sato

Keyword(s):

Spatial Frequency ◽

Lateral Geniculate Nucleus ◽

Frequency Tuning ◽

Dorsal Lateral Geniculate Nucleus ◽

Gabaergic Inhibition ◽

Spatial Frequency Tuning ◽

Lateral Geniculate ◽

Dorsal Lateral Geniculate

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Epibatidine Blocks Eye-Specific Segregation in Ferret Dorsal Lateral Geniculate Nucleus during Stage III Retinal Waves

PLoS ONE ◽

10.1371/journal.pone.0118783 ◽

2015 ◽

Vol 10 (3) ◽

pp. e0118783 ◽

Cited By ~ 2

Author(s):

Zachary W. Davis ◽

Chao Sun ◽

Brittany Derieg ◽

Barbara Chapman ◽

Hwai-Jong Cheng

Keyword(s):

Lateral Geniculate Nucleus ◽

Dorsal Lateral Geniculate Nucleus ◽

Stage Iii ◽

Retinal Waves ◽

Lateral Geniculate ◽

Dorsal Lateral Geniculate

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Nell2 regulates the contralateral-versus-ipsilateral visual projection as a layer-specific positional cue

10.1101/392597 ◽

2018 ◽

Author(s):

Chizu Nakamoto ◽

Elaine Durward ◽

Masato Horie ◽

Masaru Nakamoto

Keyword(s):

Axon Guidance ◽

Dorsal Lateral Geniculate Nucleus ◽

Retinal Ganglion ◽

Guidance Cue ◽

Retinal Axons ◽

Visual Projection ◽

Summary Statement ◽

Retinogeniculate Projection ◽

Dorsal Lateral Geniculate

SUMMARY STATEMENTNell2 is an ipsilateral layer-specific axon guidance cue in the visual thalamus and contributes to establishment of the eye-specific retinogeniculate projection by specifically inhibiting contralateral retinal axons.ABSTRACTIn mammals with binocular vision, retinal ganglion cell (RGC) axons from each eye project to eye-specific layers in the contralateral and ipsilateral dorsal lateral geniculate nucleus (dLGN). Although layer-specific axon guidance cues that discriminate contralateral and ipsilateral RGC axons have long been postulated as a key mechanism for development of the eye-specificretinogeniculate projection, the molecular nature of such cues has remained elusive. Here we show that the extracellular glycoprotein Nell2 (also known as Nel) is expressed in the dorsomedial region of the dLGN, which corresponds to the layer receiving ipsilateral RGC axons. In Nell2 mutant mice, contralateral RGC axons invaded the ipsilateral layer of the dLGN, and ipsilateral axons terminated in partially fragmented patches, forming a mosaic pattern of contralateral and ipsilateral axon termination zones. In vitro, Nell2 exerted inhibitory effects on contralateral, but not ipsilateral, RGC axons. These results provide evidence that Nell2 acts as a layer-specific positional label in the dLGN that discriminates contralateral and ipsilateral RGC axons, and that it plays essential roles in establishment of the eye-specific projection patterns in the retinogeniculate system.

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CaV3.2 KO mice have altered retinal waves but normal direction selectivity

Visual Neuroscience ◽

10.1017/s0952523814000364 ◽

2015 ◽

Vol 32 ◽

Cited By ~ 6

Author(s):

AARON M. HAMBY ◽

JULIANA M. ROSA ◽

CHING-HSIU HSU ◽

MARLA B. FELLER

Keyword(s):

Action Potentials ◽

Ganglion Cells ◽

Direction Selectivity ◽

Dorsal Lateral Geniculate Nucleus ◽

Retinal Waves ◽

Retinal Projections ◽

Temporal Properties ◽

Time Period ◽

Eye Opening ◽

Dorsal Lateral Geniculate

AbstractEarly in development, before the onset of vision, the retina establishes direction-selective responses. During this time period, the retina spontaneously generates bursts of action potentials that propagate across its extent. The precise spatial and temporal properties of these “retinal waves” have been implicated in the formation of retinal projections to the brain. However, their role in the development of direction selective circuits within the retina has not yet been determined. We addressed this issue by combining multielectrode array and cell-attached recordings to examine mice that lack the CaV3.2 subunit of T-type Ca2+ channels (CaV3.2 KO) because these mice exhibit disrupted waves during the period that direction selective circuits are established. We found that the spontaneous activity of these mice displays wave-associated bursts of action potentials that are altered from that of control mice: the frequency of these bursts is significantly decreased and the firing rate within each burst is reduced. Moreover, the projection patterns of the retina demonstrate decreased eye-specific segregation in the dorsal lateral geniculate nucleus (dLGN). However, after eye-opening, the direction selective responses of CaV3.2 KO direction selective ganglion cells (DSGCs) are indistinguishable from those of wild-type DSGCs. Our data indicate that although the temporal properties of the action potential bursts associated with retinal waves are important for activity-dependent refining of retinal projections to central targets, they are not critical for establishing direction selectivity in the retina.

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The role of retinogeniculate afferents in the development of connections between visual cortex and the dorsal lateral geniculate nucleus

Developmental Brain Research ◽

10.1016/0165-3806(83)90118-9 ◽

1983 ◽

Vol 10 (1) ◽

pp. 33-39 ◽

Cited By ~ 11

Author(s):

Judy K. Brunso-Bechtold ◽

Sherre L. Florence ◽

Vivien A. Casagrande

Keyword(s):

Visual Cortex ◽

Lateral Geniculate Nucleus ◽

Dorsal Lateral Geniculate Nucleus ◽

Lateral Geniculate ◽

Dorsal Lateral Geniculate

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The role of nitric oxide in the transformation of visual information within the dorsal lateral geniculate nucleus of the cat

Neuropharmacology ◽

10.1016/0028-3908(94)90043-4 ◽

1994 ◽

Vol 33 (11) ◽

pp. 1413-1418 ◽

Cited By ~ 30

Author(s):

J. Cudeiro ◽

K.L. Grieve ◽

C. Rivadulla ◽

R. Rodríguez ◽

S. Martínez-Conde ◽

...

Keyword(s):

Nitric Oxide ◽

Lateral Geniculate Nucleus ◽

Visual Information ◽

Dorsal Lateral Geniculate Nucleus ◽

Lateral Geniculate ◽

Dorsal Lateral Geniculate

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Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Visual Neuroscience ◽

10.1017/s0952523810000386 ◽

2011 ◽

Vol 28 (2) ◽

pp. 175-181 ◽

Cited By ~ 7

Author(s):

BRADLY Q. VO ◽

A. JOSEPH BLOOM ◽

SUSAN M. CULICAN

Keyword(s):

Normal Development ◽

Ganglion Cells ◽

Dorsal Lateral Geniculate Nucleus ◽

Retinal Ganglion ◽

Topographic Map ◽

Local Refinement ◽

Retinal Axons ◽

Retinogeniculate Projection ◽

Dorsal Lateral Geniculate ◽

Retinocollicular Projection

AbstractPrecise targeting of retinal projections is required for the normal development of topographic maps in the mammalian primary visual system. During development, retinal axons project to and occupy topographically appropriate positions in the dorsal lateral geniculate nucleus (dLGN) and superior colliculus (SC). Phr1 retinal mutant mice, which display mislocalization of the ipsilateral retinogeniculate projection independent of activity and ephrin-A signaling, were found to have a more global disruption of topographic specificity of retinofugal inputs. The retinocollicular projection lacks local refinement of terminal zones and multiple ectopic termination zones originate from the dorsal–nasal (DN) retinal quadrant. Similarly, in the dLGN, the inputs originating from the contralateral DN retina are poorly refined in the Phr1 mutant. These results show that Phr1 is an essential regulator of retinal ganglion cell projection during both dLGN and SC topographic map development.

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