Development of Precise Maps in Visual Cortex Requires Patterned Spontaneous Activity in the Retina

Cang, Jianhua; Renterı́a, René C.; Kaneko, Megumi; Liu, Xiaorong; Copenhagen, David R.; Stryker, Michael P.

doi:10.1016/j.neuron.2005.09.015

Cited by 272 publications

(292 citation statements)

References 49 publications

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“…Tuning curves in Figures 2 and 3 were fit with a cosine-wave function. To measure OD, we used a standard metric (Cang et al, 2005;Priebe, 2008) as follows:…”

Section: Methodsmentioning

confidence: 99%

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1

2017

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Experiences during the critical period sculpt the circuitry within the neocortex, leading to changes in the functional responses of sensory neurons. Monocular deprivation (MD) during the visual critical period causes shifts in ocular preference, or dominance, toward the open eye in primary visual cortex (V1) and disrupts the normal development of acuity. In carnivores and primates, MD also disrupts the emergence of binocular disparity selectivity, a cue resulting from integrating ocular inputs. This disruption may be a result of the increase in neurons driven exclusively by the open eye that follows deprivation or a result of a mismatch in the convergence of ocular inputs. To distinguish between these possibilities, we measured the ocular dominance (OD) and disparity selectivity of neurons from male and female mouse V1 following MD. Normal mouse V1 neurons are dominated by contralateral eye input and contralateral eye deprivation shifts mouse V1 neurons toward more balanced responses between the eyes. This shift toward binocularity, as assayed by OD, decreased disparity sensitivity. MD did not alter the initial maturation of binocularity, as disparity selectivity before the MD was indistinguishable from normal mature animals. Decreased disparity tuning was most pronounced in binocular and ipsilaterally biased neurons, which are the populations that have undergone the largest shifts in OD. In concert with the decline in disparity selectivity, we observed a shift toward lower spatial frequency selectivity for the ipsilateral eye following MD. These results suggest an emergence of novel synaptic inputs during MD that disrupt the representation of disparity selectivity.

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“…Tuning curves in Figures 2 and 3 were fit with a cosine-wave function. To measure OD, we used a standard metric (Cang et al, 2005;Priebe, 2008) as follows:…”

Section: Methodsmentioning

confidence: 99%

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1

2017

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“…Also, blockade of spontaneous retinal activity by tetrodotoxin around the time of eye opening, or visual deprivation after 1 week of vision, disrupted synaptic strengthening and pruning of excess retinal afferents in LGN (Hooks and Chen, 2006). These above studies indicate that early spontaneous activity in the eye or visual experience could alter the synaptic connections in higher visual centers, yet little is known of the underlying molecular mechanism (Cang et al, 2005;Hooks and Chen, 2006). Interestingly, exogenous BDNF protein injected into a visually deprived eye, or reduced endogenous BDNF expression in the nondeprived eye, was found to counteract the ocular dominance shift induced by eyelid closure (Mandolesi et al, 2005).…”

Section: Age-and Experience-dependent Maturation Of Different Subtypementioning

confidence: 99%

“…Our results raise an interesting question of whether activity and BDNF signaling via TrkB receptors in retina play a role in regulating the plasticity of higher visual centers. In mouse, development of precise maps in visual cortex was shown to require patterned spontaneous activity in retina (Cang et al, 2005). Also, blockade of spontaneous retinal activity by tetrodotoxin around the time of eye opening, or visual deprivation after 1 week of vision, disrupted synaptic strengthening and pruning of excess retinal afferents in LGN (Hooks and Chen, 2006).…”

Section: Age-and Experience-dependent Maturation Of Different Subtypementioning

confidence: 99%

Brain-Derived Neurotrophic Factor and TrkB Modulate Visual Experience-Dependent Refinement of Neuronal Pathways in Retina

et al. 2007

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Sensory experience refines neuronal structure and functionality. The visual system has proved to be a productive model system to study this plasticity. In the neonatal retina, the dendritic arbors of a large proportion of ganglion cells are diffuse in the inner plexiform layer. With maturation, many of these arbors become monolaminated. Visual deprivation suppresses this remodeling. Little is known of the molecular mechanisms controlling maturational and experience-dependent refinement. Here, we tested the hypothesis that brainderived neurotrophic factor (BDNF), which is known to regulate dendritic branching and synaptic function in the brain, modulates the developmental and visual experience-dependent refinement of retinal ganglion cells. We used a transgenic mouse line, in which a small number of ganglion cells were labeled with yellow fluorescence protein, to delineate their dendritic structure in vivo. We found that transgenic overexpression of BDNF accelerated the laminar refinement of ganglion cell dendrites, whereas decreased TrkB expression or retina-specific deletion of TrkB, the cognate receptor for BDNF, retarded it. BDNF-TrkB signaling regulated the maturational formation of new branches in ON but not the bilaminated ON-OFF ganglion cells. Furthermore, BDNF overexpression overrides the requirement for visual inputs to stimulate laminar refinement and dendritic branching of ganglion cells. These experiments reveal a previously unrecognized action of BDNF and TrkB in controlling cell-specific, experience-dependent remodeling of neuronal structures in the visual system.

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“…During the first postnatal week in mice, correlations in retinal ganglion cell (RGC) firing arise from nicotinic acetylcholine receptor (nAChR)-dependent retinal waves; in the absence of the ␤2 subunit of this receptor, waves are disrupted, resulting in minor N-T topographic mapping errors in both the retinocollicular and retinogeniculate projections (Rossi et al, 2001;Grubb et al, 2003;McLaughlin et al, 2003;Cang et al, 2005b;Chandrasekaran et al, 2005). These mapping errors raise the possibility that the remaining topography observed in ephrin-A2/A5 double knock-outs (dkos) could be partly attributable to the presence of patterned retinal activity.…”

Section: Introductionmentioning

confidence: 99%

Ephrin-As and Patterned Retinal Activity Act Together in the Development of Topographic Maps in the Primary Visual System

Pfeiffenberger

Yamada²,

Feldheim³

2006

J. Neurosci.

152

185

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The development of topographic maps in the primary visual system is thought to rely on a combination of EphA/ephrin-A interactions and patterned neural activity. Here, we characterize the retinogeniculate and retinocollicular maps of mice mutant for ephrins-A2, -A3, and -A5 (the three ephrin-As expressed in the mouse visual system), mice mutant for the ␤2 subunit of the nicotinic acetylcholine receptor (that lack early patterned retinal activity), and mice mutant for both ephrin-As and ␤2. We also provide the first comprehensive anatomical description of the topographic connections between the retina and the dorsal lateral geniculate nucleus. We find that, although ephrin-A2/A3/A5 triple knock-out mice have severe mapping defects in both projections, they do not completely lack topography. Mice lacking ␤2-dependent retinal activity have nearly normal topography but fail to refine axonal arbors. Mice mutant for both ephrin-As and ␤2 have synergistic mapping defects that result in a near absence of map in the retinocollicular projection; however, the retinogeniculate projection is not as severely disrupted as the retinocollicular projection is in these mutants. These results show that ephrin-As and patterned retinal activity act together to establish topographic maps, and demonstrate that midbrain and forebrain connections have a differential requirement for ephrin-As and patterned retinal activity in topographic map development.

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Development of Precise Maps in Visual Cortex Requires Patterned Spontaneous Activity in the Retina

Cited by 272 publications

References 49 publications

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1

Binocular Disparity Selectivity Weakened after Monocular Deprivation in Mouse V1

Brain-Derived Neurotrophic Factor and TrkB Modulate Visual Experience-Dependent Refinement of Neuronal Pathways in Retina

Ephrin-As and Patterned Retinal Activity Act Together in the Development of Topographic Maps in the Primary Visual System

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