Dynamics of Spontaneous Activity in the Fetal Macaque Retina during Development of Retinogeniculate Pathways

Warland, David K.; Huberman, Andrew D.; Chalupa, Leo M.

doi:10.1523/jneurosci.0328-06.2006

Cited by 54 publications

(42 citation statements)

References 33 publications

(54 reference statements)

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“…The tissue preparation and MEA recording procedures were similar to that described (36). Briefly, after euthanasia the eyes were enucleated, and the retinas were isolated and stored in buffered and oxygenated Minimum Essential Medium Eagle (MEME) (M7278; Sigma-Aldrich) at room temperature.…”

Section: Methodsmentioning

confidence: 99%

Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor

Sun¹,

Warland²,

Ballesteros³

et al. 2008

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

110

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The structural and functional properties of the visual system are disrupted in mutant animals lacking the ␤2 subunit of the nicotinic acetylcholine receptor. In particular, eye-specific retinogeniculate projections do not develop normally in these mutants. It is widely thought that the developing retinas of ␤2 ؊/؊ mutants do not manifest correlated activity, leading to the notion that retinal waves play an instructional role in the formation of eye-specific retinogeniculate projections. By multielectrode array recordings, we show here that the ␤2 ؊/؊ mutants have robust retinal waves during the formation of eye-specific projections. Unlike in WT animals, however, the mutant retinal waves are propagated by gap junctions rather than cholinergic circuitry. These results indicate that lack of retinal waves cannot account for the abnormalities that have been documented in the retinogeniculate pathway of the ␤2 ؊/؊ mutants and suggest that other factors must contribute to the deficits in the visual system that have been noted in these animals.lateral geniculate nucleus ͉ multielectrode array ͉ retinal ganglion cells ͉ retinogeniculate segregation ͉ gap junction T he precise connections that characterize the mature nervous system often arise from an early exuberant pattern that becomes refined through a combination of molecular and activity-dependent cues. In the case of the visual system, the projections of the two eyes to the dorsal lateral geniculate nucleus (dLGN) are initially intermingled before gradually becoming segregated into separate layers in animals with a laminated dLGN such as ferret, cat, and monkey or to different regions of the geniculate as in the mouse and rat (1-3). During the developmental period when eye-specific retinogeniculate projections are being established the retina manifests a remarkable pattern of activity. Immature retinal ganglion cells (RGCs) discharge periodic bursts of action potentials, with adjacent cells firing in a temporally correlated manner, resulting in waves of activity sweeping across the retinal surface (4-7). These retinal waves have been considered to be essential for the formation of eye-specific retinogeniculate projections through a Hebbiantype mechanism where the connections stemming from one eye are strengthened and maintained, whereas those of the other eye become eliminated based on which set of inputs is more capable of activating dLGN neurons (8, 9). Evidence in support of this prevalent notion has been provided by studies that have relied on pharmacological agents to alter the normal activity patterns of the developing retina. Several studies have shown that blocking or perturbing retinal activity prevents the formation of segregated retinogeniculate projections (9-11). These observations have led to the conclusion that retinal waves instruct the formation of eye-specific domains (8,(12)(13)(14).Studies that have used mutant mice have also supported a linkage between retinal waves and development of segregated retinogeniculate projections. In particular, anim...

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Section: Methodsmentioning

confidence: 99%

Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor

Sun¹,

Warland²,

Ballesteros³

et al. 2008

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

110

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show abstract

“…Waves initiate from random locations in the retina and propagate over spatially restricted domains such that over time the whole retina is tiled by locally correlated activity (Feller et al 1996(Feller et al , 1997. Retinal waves have been found in chickens, turtles, mice, ferrets, and monkeys (Warland et al 2006,Wong 1999. In some species, such as primates, waves occur only prenatally, whereas in other species, such as mice and ferrets, they occur both prenatally and postnatally.…”

Section: Neural Activitymentioning

confidence: 99%

Mechanisms Underlying Development of Visual Maps and Receptive Fields

Huberman

Feller

Chapman

2008

Annu. Rev. Neurosci.

556

617

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Patterns of synaptic connections in the visual system are remarkably precise. These connections dictate the receptive field properties of individual visual neurons and ultimately determine the quality of visual perception. Spontaneous neural activity is necessary for the development of various receptive field properties and visual feature maps. In recent years, attention has shifted to understanding the mechanisms by which spontaneous activity in the developing retina, lateral geniculate nucleus, and visual cortex instruct the axonal and dendritic refinements that give rise to orderly connections in the visual system. Axon guidance cues and a growing list of other molecules, including immune system factors, have also recently been implicated in visual circuit wiring. A major goal now is to determine how these molecules cooperate with spontaneous and visually evoked activity to give rise to the circuits underlying precise receptive field tuning and orderly visual maps.

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“…One possibility is that this partitioning resulted not only from molecular specification but in addition from activity-dependent self-organization (39). Long before visual experience is available, waves of correlated activity travel over the retina and contribute to the establishment of neighborhood relations in the LGN (20,21,(40)(41)(42)(43).…”

Section: Visual Field Maps In Lgnmentioning

confidence: 99%

Bilateral visual field maps in a patient with only one hemisphere

Muckli

Naumer

Singer

2009

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

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In mammals smooth retinotopic maps of the visual field are formed along the visual processing pathway whereby the left visual field is represented in the right hemisphere and vice versa. The reorganization of retinotopic maps in the lateral geniculate nucleus (LGN) of the thalamus and early visual areas (V1-V3) is studied in a patient who was born with only one cerebral hemisphere. Before the seventh week of embryonic gestation, the development of the patient's right cerebral hemisphere terminated. Despite the complete loss of her right hemisphere (di-and telencephalon) at birth, the patient's remaining hemisphere has not only developed maps of the contralateral (right) visual hemifield but, surprisingly, also maps of the ipsilateral (left) visual hemifield. Retinal ganglion-cells changed their predetermined crossing pattern in the optic chiasm and grew to the ipsilateral LGN. In the visual cortex, islands of ipsilateral visual field representations were located along the representations of the vertical meridian. In V1, smooth and continuous maps from contra-and ipsilateral hemifield overlap each other, whereas in ventral V2 and V3 ipsilateral quarter field representations invaded small distinct cortical patches. This reveals a surprising flexibility of the self-organizing developmental mechanisms responsible for map formation.functional MRI ͉ retinotopic mapping ͉ achiasmatic ͉ cortical lesion ͉ V1 development

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Dynamics of Spontaneous Activity in the Fetal Macaque Retina during Development of Retinogeniculate Pathways

Cited by 54 publications

References 33 publications

Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor

Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor

Mechanisms Underlying Development of Visual Maps and Receptive Fields

Bilateral visual field maps in a patient with only one hemisphere

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