Home LiteratureArticle Details
PMID: 17046688 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Spontaneous retinal activity mediates development of ocular dominance columns and binocular receptive fields in v1.

Neuron ·Vol. 52 ·No. 2 ·2006-10-19 ·Pages 247-54

Huberman AD, Speer CM, Chapman B

Abstract

The mechanisms that give rise to ocular dominance columns (ODCs) during development are controversial. Early experiments indicated a key role for retinal activity in ODC formation. However, later studies showed that in those early experiments, the retinal activity perturbation was initiated after ODCs had already formed. Moreover, recent studies concluded that early eye removals do not impact ODC segregation. Here we blocked spontaneous retinal activity during the very early stages of ODC development. This permanently disrupted the anatomical organization of ODCs and led to a dramatic increase in receptive field size for binocular cells in primary visual cortex. Our data suggest that early spontaneous retinal activity conveys crucial information about whether thalamocortical axons represent one or the other eye and that this activity mediates binocular competition important for shaping receptive fields in primary visual cortex.

MeSH Terms
Action Potentials/physiology Aging/physiology Animals Animals, Newborn Bridged Bicyclo Compounds, Heterocyclic/pharmacology Cell Communication/physiology Cell Differentiation/physiology Cues Dominance, Ocular/physiology Ferrets Geniculate Bodies/cytology,growth & development Neuronal Plasticity/physiology Nicotinic Agonists/pharmacology Pyridines/pharmacology Retina/cytology,growth & development Synaptic Transmission/physiology Vision, Binocular/physiology Visual Cortex/cytology,growth & development Visual Fields/physiology Visual Pathways/cytology,growth & development
Chemicals
Bridged Bicyclo Compounds, Heterocyclic Nicotinic Agonists Pyridines epibatidine
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Huberman Andrew D
Center for Neuroscience, University of California, Davis, Davis, California 95616, USA.
Speer Colenso M
Chapman Barbara
References (43)
43 references, click to expand
  1. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina.
    Neuron. 2005 Dec 8;48(5):797-809 PMID: 16337917
  2. Retinal waves trigger spindle bursts in the neonatal rat visual cortex.
    J Neurosci. 2006 Jun 21;26(25):6728-36 PMID: 16793880
  3. Monocular cells without ocular dominance columns.
    J Neurophysiol. 2006 Nov;96(5):2253-64 PMID: 16855115
  4. Ephrin-as guide the formation of functional maps in the visual cortex.
    Neuron. 2005 Nov 23;48(4):577-89 PMID: 16301175
  5. Ephrin-As mediate targeting of eye-specific projections to the lateral geniculate nucleus.
    Nat Neurosci. 2005 Aug;8(8):1013-21 PMID: 16025110
  6. Competition in retinogeniculate patterning driven by spontaneous activity.
    Science. 1998 Mar 27;279(5359):2108-12 PMID: 9516112
  7. The use of m-sequences in the analysis of visual neurons: linear receptive field properties.
    Vis Neurosci. 1997 Nov-Dec;14(6):1015-27 PMID: 9447685
  8. The role of visual experience in the development of columns in cat visual cortex.
    Science. 1998 Jan 23;279(5350):566-70 PMID: 9438851
  9. Development and organization of ocular dominance bands in primary visual cortex of the sable ferret.
    J Comp Neurol. 1999 May 3;407(2):151-65 PMID: 10213088
  10. Correlational structure of spontaneous neuronal activity in the developing lateral geniculate nucleus in vivo.
    Science. 1999 Jul 23;285(5427):599-604 PMID: 10417392
  11. The critical period for ocular dominance plasticity in the Ferret's visual cortex.
    J Neurosci. 1999 Aug 15;19(16):6965-78 PMID: 10436053
  12. Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex.
    Nature. 2005 Feb 10;433(7026):597-603 PMID: 15660108
  13. Receptive fields, binocular interaction and functional architecture in the cat's visual cortex.
    J Physiol. 1962 Jan;160:106-54 PMID: 14449617
  14. Maps of central visual space in ferret V1 and V2 lack matching inputs from the two eyes.
    J Neurosci. 1999 Aug 15;19(16):7089-99 PMID: 10436063
  15. Development of ocular dominance columns in the absence of retinal input.
    Nat Neurosci. 1999 Dec;2(12):1125-30 PMID: 10570491
  16. Necessity for afferent activity to maintain eye-specific segregation in ferret lateral geniculate nucleus.
    Science. 2000 Mar 31;287(5462):2479-82 PMID: 10741966
  17. Early development of ocular dominance columns.
    Science. 2000 Nov 17;290(5495):1321-4 PMID: 11082053
  18. Emergence of ocular dominance columns in cat visual cortex by 2 weeks of age.
    J Comp Neurol. 2001 Feb 5;430(2):235-49 PMID: 11135259
  19. Requirement of the nicotinic acetylcholine receptor beta 2 subunit for the anatomical and functional development of the visual system.
    Proc Natl Acad Sci U S A. 2001 May 22;98(11):6453-8 PMID: 11344259
  20. Spontaneous activity in developing ferret visual cortex in vivo.
    J Neurosci. 2001 Nov 15;21(22):8906-14 PMID: 11698602
  21. Retinogeniculate axons undergo eye-specific segregation in the absence of eye-specific layers.
    J Neurosci. 2002 Jul 1;22(13):5259-64 PMID: 12097474
  22. Decoupling eye-specific segregation from lamination in the lateral geniculate nucleus.
    J Neurosci. 2002 Nov 1;22(21):9419-29 PMID: 12417667
  23. Capricious expression of cortical columns in the primate brain.
    Nat Neurosci. 2003 Feb;6(2):113-4 PMID: 12536211
  24. Receptive fields and response properties of neurons in layer 4 of ferret visual cortex.
    J Neurophysiol. 2003 Feb;89(2):1003-15 PMID: 12574476
  25. Role of subplate neurons in functional maturation of visual cortical columns.
    Science. 2003 Jul 25;301(5632):521-5 PMID: 12881571
  26. Retinotopic map refinement requires spontaneous retinal waves during a brief critical period of development.
    Neuron. 2003 Dec 18;40(6):1147-60 PMID: 14687549
  27. Abnormal functional organization in the dorsal lateral geniculate nucleus of mice lacking the beta 2 subunit of the nicotinic acetylcholine receptor.
    Neuron. 2003 Dec 18;40(6):1161-72 PMID: 14687550
  28. Autoradiographic demonstration of ocular-dominance columns in the monkey striate cortex by means of transneuronal transport.
    Brain Res. 1974 Oct 18;79(2):273-9 PMID: 4423575
  29. Prenatal genesis of connections subserving ocular dominance in the rhesus monkey.
    Nature. 1976 Jun 10;261(5560):467-71 PMID: 819835
  30. The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development.
    J Comp Neurol. 1981 Dec 1;203(2):189-211 PMID: 7309920
  31. The complete pattern of ocular dominance stripes in the striate cortex and visual field of the macaque monkey.
    J Neurosci. 1985 Feb;5(2):486-501 PMID: 3973679
  32. The organization of the lateral geniculate nucleus and of the geniculocortical pathway that develops without retinal afferents.
    Brain Res. 1985 Jun;352(2):221-33 PMID: 4027668
  33. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex.
    J Neurosci. 1986 Aug;6(8):2117-33 PMID: 3746403
  34. Segregation of ON and OFF afferents to ferret visual cortex.
    J Neurophysiol. 1988 May;59(5):1410-29 PMID: 3385467
  35. Organization of primary visual cortex (area 17) in the ferret.
    J Comp Neurol. 1988 Dec 8;278(2):157-80 PMID: 3068264
  36. Ocular dominance column development: analysis and simulation.
    Science. 1989 Aug 11;245(4918):605-15 PMID: 2762813
  37. Involvement of subplate neurons in the formation of ocular dominance columns.
    Science. 1992 Mar 13;255(5050):1441-3 PMID: 1542795
  38. Transient period of correlated bursting activity during development of the mammalian retina.
    Neuron. 1993 Nov;11(5):923-38 PMID: 8240814
  39. Ocular dominance column development: strabismus changes the spacing of adjacent columns in cat visual cortex.
    J Neurosci. 1994 Dec;14(12):7451-68 PMID: 7996187
  40. Ultrastructural evidence for synaptic interactions between thalamocortical axons and subplate neurons.
    Eur J Neurosci. 1994 Nov 1;6(11):1729-42 PMID: 7874312
  41. Ocular dominance columns and their development in layer IV of the cat's visual cortex: a quantitative study.
    J Comp Neurol. 1978 May 1;179(1):223-44 PMID: 8980725
  42. Ephrin-As and neural activity are required for eye-specific patterning during retinogeniculate mapping.
    Nat Neurosci. 2005 Aug;8(8):1022-7 PMID: 16025107
  43. A precritical period for plasticity in visual cortex.
    Curr Opin Neurobiol. 2005 Feb;15(1):94-100 PMID: 15721750
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
0896-6273
Published
2006-10-19
Pages
247-54
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC2647846
Subset
IM
Grants
NEI NIH HHS · R01 EY011369 · United States
NEI NIH HHS · R01 EY011369-11 · United States
Corrections
CommentIn
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]