Competition in Retinogeniculate Patterning Driven by Spontaneous Activity
Abstract
When contacts are first forming in the developing nervous system, many neurons generate spontaneous activity that has been hypothesized to shape appropriately patterned connections. In Mustela putorius furo, monocular intraocular blockade of spontaneous retinal waves of action potentials by cholinergic agents altered the subsequent eye-specific lamination pattern of the lateral geniculate nucleus (LGN). The projection from the active retina was greatly expanded into territory normally belonging to the other eye, and the projection from the inactive retina was substantially reduced. Thus, interocular competition driven by endogenous retinal activity determines the pattern of eye-specific connections from retina to LGN, demonstrating that spontaneous activity can produce highly stereotyped patterns of connections before the onset of visual experience.
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Monocular epibatidine injection preserves eye-specific segregation and induces the affected weaker projections to lose their territory preferentially.
“Previous work has shown that injecting epibatidine binocularly blocks eye-specific segregation in dLGN, whereas injecting epibatidine monocularly preserves eye-specific segregation, inducing the affected weaker projections to lose their territory preferentially.”
From Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways (2013) · cites this paper as [17]
Retinogeniculate segregation does not occur when retinal wave activity is blocked.
“Retinogeniculate segregation does not occur when retinal wave activity is blocked17,24 raising the question of whether neural activity plays a role in astrocyte-mediated synapse elimination.”
From Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways (2013) · cites this paper as [17]
Binocular epibatidine injection blocks eye-specific segregation in dLGN.
“Previous work has shown that injecting epibatidine binocularly blocks eye-specific segregation in dLGN, whereas injecting epibatidine monocularly preserves eye-specific segregation, inducing the affected weaker projections to lose their territory preferentially.”
From Astrocytes mediate synapse elimination through MEGF10 and MERTK pathways (2013) · cites this paper as [17]
Cites
Patterned Activity, Synaptic Convergence, and the NMDA Receptor in Developing Visual Pathways
Constantine-Paton, M., Cline, H. T., & Debski, E. (1990) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.13.030190.001021 · Cited by 784 · see citing works
Impulse activity and the patterning of connections during cns development
Shatz, C. J. (1990) · Neuron · doi:10.1016/0896-6273(90)90333-b · Cited by 766 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089 · see citing works
“(Del Rio and Feller, 2006; Feller, 1999; Penn et al., 1998; Shatz, 1990; Torborg and Feller, 2005).”
InfluentialAstrocytes mediate synapse elimination through MEGF10 and MERTK pathways
Chung, W.-S., Clarke, L. E., Wang, G. X., Stafford, B. K., Sher, A., Chakraborty, C., Joung, J., Foo, L. C., Thompson, A., Chen, C., et al. (2013) · Nature · doi:10.1038/nature12776 · Cited by 1,377 · see citing works
“Retinogeniculate segregation does not occur when retinal wave activity is blocked 17,24 raising the question of whether neural activity plays a role in astrocyte-mediated synapse elimination.”
InfluentialNEUROTROPHINS AND SYNAPTIC PLASTICITY
McAllister, A. K., Katz, L. C., & Lo, D. C. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.295 · Cited by 1,337 · see citing works
Hensch, T. K. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144327 · Cited by 1,300 · see citing works
The Complement System: An Unexpected Role in Synaptic Pruning During Development and Disease
Stephan, A. H., Barres, B. A., & Stevens, B. (2012) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-061010-113810 · Cited by 1,113 · see citing works
Flavell, S. W., & Greenberg, M. E. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125631 · Cited by 832 · see citing works
Astrocytes Control Synapse Formation, Function, and Elimination
Chung, W.-S., Allen, N. J., & Eroglu, C. (2015) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a020370 · Cited by 839 · see citing works
Functional requirement for class I MHC in CNS development and plasticity
Huh, G. S., Boulanger, L. M., Du, H., Riquelme, P. A., Brotz, T. M., & Shatz, C. J. (2000) · Science · doi:10.1126/science.290.5499.2155 · Cited by 828 · see citing works
Self-citationEssential Role for TrkB Receptors in Hippocampus-Mediated Learning
Minichiello, L., Korte, M., Wolfer, D., Kühn, R., Unsicker, K., Cestari, V., Rossi-Arnaud, C., Lipp, H.-P., Bonhoeffer, T., & Klein, R. (1999) · Neuron · doi:10.1016/s0896-6273(00)80853-3 · Cited by 799 · see citing works
Mechanisms underlying development of visual maps and receptive fields
Huberman, A. D., Feller, M. B., & Chapman, B. (2008) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.31.060407.125533 · Cited by 628 · see citing works
Self-citationThe “quad‐partite” synapse: Microglia‐synapse interactions in the developing and mature CNS
Schafer, D. P., Lehrman, E. K., & Stevens, B. (2013) · Glia · doi:10.1002/glia.22389 · Cited by 570 · see citing works
Retinal waves and visual system development
Wong, R. O. L. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.29 · Cited by 544 · see citing works
Retinal waves coordinate patterned activity throughout the developing visual system
Ackman, J. B., Burbridge, T. J., & Crair, M. C. (2012) · Nature · doi:10.1038/nature11529 · Cited by 525 · see citing works
Large-scale oscillatory calcium waves in the immature cortex
Garaschuk, O., Linn, J., Eilers, J., & Konnerth, A. (2000) · Nature Neuroscience · doi:10.1038/74823 · Cited by 493 · see citing works
McLaughlin, T., Torborg, C. L., Feller, M. B., & O'Leary, D. D. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00790-6 · Cited by 422 · see citing works
Self-citationArchitectures of neuronal circuits
Luo, L. (2021) · Science · doi:10.1126/science.abg7285 · Cited by 390 · see citing works
Bansal, A., Singer, J. H., Hwang, B. J., Xu, W., Beaudet, A., & Feller, M. B. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-20-07672.2000 · Cited by 350 · see citing works
Self-citationAn instructive role for retinal waves in the development of retinogeniculate connectivity
Stellwagen, D., & Shatz, C. J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00577-9 · Cited by 342 · see citing works
Self-citationSpontaneous correlated activity in developing neural circuits
Feller, M. B. (1999) · Neuron · doi:10.1016/s0896-6273(00)80724-2 · Cited by 342 · see citing works
Self-citationNeuron-glia signaling in synapse elimination
Wilton, D. K., Dissing-Olesen, L., & Stevens, B. (2019) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-070918-050306 · Cited by 332 · see citing works
Distinct roles for spontaneous and visual activity in remodeling of the retinogeniculate synapse
Hooks, B. M., & Chen, C. (2006) · Neuron · doi:10.1016/j.neuron.2006.07.007 · Cited by 311 · see citing works
Development of precise maps in visual cortex requires patterned spontaneous activity in the retina
Cang, J., Rentería, R. C., Kaneko, M., Liu, X., Copenhagen, D. R., & Stryker, M. P. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.015 · Cited by 306 · see citing works
Neuronal activity is required for the development of specific cortical interneuron subtypes
De Marco García, N. V., Karayannis, T., & Fishell, G. (2011) · Nature · doi:10.1038/nature09865 · Cited by 294 · see citing works
Synapse elimination and learning rules co-regulated by MHC class I H2-Db
Lee, H., Brott, B. K., Kirkby, L. A., Adelson, J. D., Cheng, S., Feller, M. B., Datwani, A., & Shatz, C. J. (2014) · Nature · doi:10.1038/nature13154 · Cited by 228 · see citing works
Self-citationButts, D. A., Kanold, P. O., & Shatz, C. J. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050061 · Cited by 208 · see citing works
Self-citationRole of emergent neural activity in visual map development
Ackman, J. B., & Crair, M. C. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.11.011 · Cited by 219 · see citing works
Grubb, M. S., Rossi, F. M., Changeux, J.-P., & Thompson, I. D. (2003) · Neuron · doi:10.1016/s0896-6273(03)00789-x · Cited by 208 · see citing works
Classical MHCI Molecules Regulate Retinogeniculate Refinement and Limit Ocular Dominance Plasticity
Datwani, A., McConnell, M. J., Kanold, P. O., Micheva, K. D., Busse, B., Shamloo, M., Smith, S. J., & Shatz, C. J. (2009) · Neuron · doi:10.1016/j.neuron.2009.10.015 · Cited by 212 · see citing works
Self-citationPfeiffenberger, C., Cutforth, T., Woods, G., Yamada, J., Rentería, R. C., Copenhagen, D. R., Flanagan, J. G., & Feldheim, D. A. (2005) · Nature Neuroscience · doi:10.1038/nn1508 · Cited by 189 · see citing works
Chandrasekaran, A. R., Plas, D. T., Gonzalez, E., & Crair, M. C. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1470-05.2005 · Cited by 192 · see citing works
An instructive role for patterned spontaneous retinal activity in mouse visual map development
Xu, H.-P., Furman, M., Mineur, Y. S., Chen, H., King, S. L., Zenisek, D., Zhou, Z. J., Butts, D. A., Tian, N., Picciotto, M. R., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.028 · Cited by 170 · see citing works
Neuronal Pentraxins Mediate Synaptic Refinement in the Developing Visual System
Bjartmar, L., Huberman, A. D., Ullian, E. M., Renteria, R. C., Liu, X., Xu, W., Prezioso, J., Susman, M. W., Stellwagen, D., Stokes, C. C., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4212-05.2006 · Cited by 179 · see citing works
Upton, A. L., Salichon, N., Lebrand, C., Ravary, A., Blakely, R., Seif, I., & Gaspar, P. (1999) · The Journal of Neuroscience · doi:10.1523/jneurosci.19-16-07007.1999 · Cited by 173 · see citing works
Stafford, B. K., Sher, A., Litke, A. M., & Feldheim, D. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.09.021 · Cited by 156 · see citing works
The acquisition of motoneuron subtype identity and motor circuit formation
Landmesser, L. T. (2001) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(00)00090-3 · Cited by 136 · see citing works
Eye-specific retinogeniculate segregation independent of normal neuronal activity
Huberman, A. D., Wang, G.-Y., Liets, L. C., Collins, O. A., Chapman, B., & Chalupa, L. M. (2003) · Science · doi:10.1126/science.1080694 · Cited by 129 · see citing works
Atluri, P., Fleck, M. W., Shen, Q., Mah, S. J., Stadfelt, D., Barnes, W., Goderie, S. K., Temple, S., & Schneider, A. S. (2001) · Developmental Biology · doi:10.1006/dbio.2001.0453 · Cited by 110 · see citing works
Retinal waves in mice lacking the β2 subunit of the nicotinic acetylcholine receptor
Sun, C., Warland, D. K., Ballesteros, J. M., van der List, D., & Chalupa, L. M. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807178105 · Cited by 80 · see citing works
Soto, F., Ma, X., Cecil, J. L., Vo, B. Q., Culican, S. M., & Kerschensteiner, D. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.0194-12.2012 · Cited by 66 · see citing works
t Traveling Slow Waves of Neural Activity: A Novel Form of Network Activity in Developing Neocortex
Peinado, T. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-02-j0002.2000 · Cited by 68 · see citing works
Adenylate Cyclase 1 as a Key Actor in the Refinement of Retinal Projection Maps
Ravary, A., Muzerelle, A., Hervé, D., Pascoli, V., Ba-Charvet, K. N., Girault, J.-A., Welker, E., & Gaspar, P. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02228.2003 · Cited by 66 · see citing works
Early brain wiring: activity-dependent processes
Penn, A. A. (2001) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a006880 · Cited by 37 · see citing works
Furman, M., & Crair, M. C. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00943.2011 · Cited by 26 · see citing works
Initiation and Propagation of Neuronal Coactivation in the Developing Hippocampus
Bolea, S., Sanchez-Andres, J. V., Huang, X., & Wu, J.-Y. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00321.2005 · Cited by 20 · see citing works
ERK signaling is required for eye-specific retino-geniculate segregation
Naska, S., Cenni, M. C., Menna, E., & Maffei, L. (2004) · Development · doi:10.1242/dev.01212 · Cited by 14 · see citing works
Activity-dependent synaptic competition and dendrite pruning in developing mitral cells
Imai, T. (2025) · Frontiers in Neural Circuits · doi:10.3389/fncir.2025.1541926 · Cited by 4 · see citing works
- Authors
- Penn, A. A., Riquelme, P. A., Feller, M. B., & Shatz, C. J.
- Affiliations
- Howard Hughes Medical Institute (US)
- Corresponding author
- Penn, Anna A.
- Feller, Marla B.
- Venue
- Science
- Published
- 1998-03-27
- Volume
- 279
- Issue
- 5359
- Pages
- 2108-2112
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- OpenAlex
- W1975196303
- Cited by
- 514
- References
- 2
- Citations by year
- 2026: 7 · 2025: 11 · 2024: 19 · 2023: 10 · 2022: 19 · 2021: 15 · 2020: 7 · 2019: 15 · 2018: 10 · 2017: 11 · 2016: 7 · 2015: 10 · 2014: 25 · 2013: 17 · 2012: 14
- FWCI
- 23.01
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (MH 98108)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
- Keywords
- lateral geniculate nucleus, cholinergic blockade, retinotopic map, visual system development, ferrets
- MeSH terms
- Action Potentials, Animals, Animals, Newborn, Axons, Bungarotoxins, Ferrets, Geniculate Bodies, Microspheres, Peptides, Pyridines, Retina, Retinal Ganglion Cells, Visual Pathways, Nicotinic Agonists, Bridged Bicyclo Compounds, Heterocyclic, Conotoxins
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