Home LiteratureArticle Details
PMID: 12441058 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Connexin36 is essential for transmission of rod-mediated visual signals in the mammalian retina.

Neuron ·Vol. 36 ·No. 4 ·2002-11-14 ·Pages 703-12

Deans MR, Volgyi B, Goodenough DA, Bloomfield SA, Paul DL

Abstract

To examine the functions of electrical synapses in the transmission of signals from rod photoreceptors to ganglion cells, we generated connexin36 knockout mice. Reporter expression indicated that connexin36 was present in multiple retinal neurons including rod photoreceptors, cone bipolar cells, and AII amacrine cells. Disruption of electrical synapses between adjacent AIIs and between AIIs and ON cone bipolars was demonstrated by intracellular injection of Neurobiotin. In addition, extracellular recording in the knockout revealed the complete elimination of rod-mediated, on-center responses at the ganglion cell level. These data represent direct proof that electrical synapses are critical for the propagation of rod signals across the mammalian retina, and they demonstrate the existence of multiple rod pathways, each of which is dependent on electrical synapses.

MeSH Terms
Alkaline Phosphatase Amacrine Cells/cytology,metabolism Animals Connexins/deficiency,genetics Contrast Sensitivity/genetics GPI-Linked Proteins Gap Junctions/metabolism Genes, Reporter/genetics Glycine/metabolism Immunohistochemistry Interneurons/cytology,metabolism Isoenzymes/genetics Mice Mice, Knockout Photic Stimulation Presynaptic Terminals/metabolism,ultrastructure Retinal Cone Photoreceptor Cells/cytology,metabolism Retinal Ganglion Cells/cytology,metabolism Retinal Rod Photoreceptor Cells/cytology,metabolism Sensory Thresholds/physiology Synaptic Transmission/genetics Vision, Ocular/genetics beta-Galactosidase/genetics
Chemicals
Connexins GPI-Linked Proteins Isoenzymes connexin 36 Alkaline Phosphatase alkaline phosphatase, placental beta-Galactosidase Glycine
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Deans Michael R
Department of Neurobiology, Harvard Medical School, 200 Longwood Avenue, Boston, MA 02115, USA.
Volgyi Bela
Goodenough Daniel A
Bloomfield Stewart A
Paul David L
References (50)
50 references, click to expand
  1. Neurotransmitter coupling through gap junctions in the retina.
    J Neurosci. 1998 Dec 15;18(24):10594-602 PMID: 9852595
  2. Genetic diseases and gene knockouts reveal diverse connexin functions.
    Annu Rev Physiol. 1999;61:283-310 PMID: 10099690
  3. Dopamine D2 receptor-mediated modulation of rod-cone coupling in the Xenopus retina.
    J Comp Neurol. 1998 Sep 7;398(4):529-38 PMID: 9717707
  4. Rod pathways: the importance of seeing nothing.
    Trends Neurosci. 1999 Nov;22(11):497-504 PMID: 10529817
  5. An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14130-5 PMID: 10570210
  6. Gap junctions in the eye: evidence for heteromeric, heterotypic and mixed-homotypic interactions.
    Brain Res Brain Res Rev. 2000 Apr;32(1):115-20 PMID: 10751660
  7. Immunocytochemical analysis of the mouse retina.
    J Comp Neurol. 2000 Aug 14;424(1):1-23 PMID: 10888735
  8. A flattened retina-eyecup preparation suitable for electrophysiological studies of neurons visualized with trans-scleral infrared illumination.
    J Neurosci Methods. 2000 Nov 30;103(2):209-16 PMID: 11084214
  9. Expression of neuronal connexin36 in AII amacrine cells of the mammalian retina.
    J Neurosci. 2001 Jan 1;21(1):230-9 PMID: 11150340
  10. Rod vision: pathways and processing in the mammalian retina.
    Prog Retin Eye Res. 2001 May;20(3):351-84 PMID: 11286897
  11. Rod pathways in the mammalian retina use connexin 36.
    J Comp Neurol. 2001 Jul 30;436(3):336-50 PMID: 11438934
  12. Visual transmission deficits in mice with targeted disruption of the gap junction gene connexin36.
    J Neurosci. 2001 Aug 15;21(16):6036-44 PMID: 11487627
  13. Synchronous activity of inhibitory networks in neocortex requires electrical synapses containing connexin36.
    Neuron. 2001 Aug 16;31(3):477-85 PMID: 11516403
  14. Microcircuits for night vision in mouse retina.
    J Neurosci. 2001 Nov 1;21(21):8616-23 PMID: 11606649
  15. Temporal properties of the mouse cone electroretinogram.
    J Neurophysiol. 2002 Jan;87(1):42-8 PMID: 11784728
  16. Mouse horizontal cells do not express connexin26 or connexin36.
    Cell Commun Adhes. 2001;8(4-6):361-6 PMID: 12064619
  17. An attempt to analyse colour reception by electrophysiology.
    J Physiol. 1966 Aug;185(3):556-86 PMID: 5918059
  18. Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina.
    J Physiol. 1967 Feb;188(3):285-307 PMID: 6032202
  19. Gap junctions between photoreceptor cells in the vertebrate retina.
    Proc Natl Acad Sci U S A. 1973 Jun;70(6):1677-81 PMID: 4198274
  20. A bistratified amacrine cell and synaptic cirucitry in the inner plexiform layer of the retina.
    Brain Res. 1975 Feb 7;84(2):293-300 PMID: 1111833
  21. The electrical response of turtle cones to flashes and steps of light.
    J Physiol. 1974 Nov;242(3):685-727 PMID: 4449052
  22. New properties of rabbit retinal ganglion cells.
    J Physiol. 1978 Mar;276:257-76 PMID: 650447
  23. Cat cones have rod input: a comparison of the response properties of cones and horizontal cell bodies in the retina of the cat.
    J Comp Neurol. 1977 Mar 1;172(1):109-35 PMID: 838876
  24. Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits.
    J Cell Biol. 1975 Apr;65(1):192-222 PMID: 1127010
  25. Cones excite rods in the retina of the turtle.
    J Physiol. 1975 Apr;246(3):639-51 PMID: 1133790
  26. The major cell populations of the mouse retina.
    J Neurosci. 1998 Nov 1;18(21):8936-46 PMID: 9786999
  27. Tracer coupling pattern of amacrine and ganglion cells in the rabbit retina.
    J Comp Neurol. 1997 Jul 14;383(4):512-28 PMID: 9208996
  28. A comparison of receptive-field and tracer-coupling size of amacrine and ganglion cells in the rabbit retina.
    Vis Neurosci. 1997 Nov-Dec;14(6):1153-65 PMID: 9447695
  29. A novel signaling pathway from rod photoreceptors to ganglion cells in mammalian retina.
    Neuron. 1998 Sep;21(3):481-93 PMID: 9768836
  30. Light-induced modulation of coupling between AII amacrine cells in the rabbit retina.
    Vis Neurosci. 1997 May-Jun;14(3):565-76 PMID: 9194323
  31. Neuronal coupling in rod-signal pathways of the retina.
    Invest Ophthalmol Vis Sci. 1997 Feb;38(2):267-73 PMID: 9040458
  32. The properties of surround antagonism elicited by spinning windmill patterns in the mudpuppy retina.
    J Physiol. 1978 May;278:101-16 PMID: 671274
  33. A physiological and morphological study of the horizontal cell types of the rabbit retina.
    J Comp Neurol. 1982 Jul 1;208(3):288-303 PMID: 6288777
  34. Electrophysiology of retinal ganglion cells in the mouse: a study of a normally pigmented mouse and a congenic hypopigmentation mutant, pearl.
    J Neurophysiol. 1982 Oct;48(4):968-80 PMID: 7143036
  35. Immunocytochemical localization of two retinoid-binding proteins in vertebrate retina.
    J Cell Biol. 1983 Sep;97(3):703-12 PMID: 6350319
  36. A new microspectrophotometric method for measuring absorbance of rat photoreceptors.
    Vision Res. 1984;24(11):1673-6 PMID: 6533992
  37. Accumulation of (3H)glycine by cone bipolar neurons in the cat retina.
    J Comp Neurol. 1986 Aug 1;250(1):1-7 PMID: 3734165
  38. Microcircuitry of the dark-adapted cat retina: functional architecture of the rod-cone network.
    J Neurosci. 1986 Dec;6(12):3505-17 PMID: 3794785
  39. Responses to single quanta of light in retinal ganglion cells of the cat.
    Vision Res. 1971;Suppl 3:87-101 PMID: 5293890
  40. Pharmacological modulation of the rod pathway in the cat retina.
    J Neurophysiol. 1988 Jun;59(6):1657-72 PMID: 3404200
  41. Modulation of rod-cone coupling by light.
    Science. 1989 Apr 21;244(4902):352-4 PMID: 2711185
  42. Functional architecture of the mammalian retina.
    Physiol Rev. 1991 Apr;71(2):447-80 PMID: 2006220
  43. Many diverse types of retinal neurons show tracer coupling when injected with biocytin or Neurobiotin.
    Neurosci Lett. 1991 Apr 29;125(2):187-90 PMID: 1715532
  44. Dopaminergic modulation of gap junction permeability between amacrine cells in mammalian retina.
    J Neurosci. 1992 Dec;12(12):4911-22 PMID: 1281499
  45. Response properties of ganglion cells in the isolated mouse retina.
    Vis Neurosci. 1993 Jan-Feb;10(1):31-9 PMID: 8424927
  46. Photovoltage of rods and cones in the macaque retina.
    Science. 1995 May 19;268(5213):1053-6 PMID: 7754386
  47. Differential properties of two gap junctional pathways made by AII amacrine cells.
    Nature. 1995 Oct 26;377(6551):734-7 PMID: 7477263
  48. An alternative pathway for signal flow from rod photoreceptors to ganglion cells in mammalian retina.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10658-62 PMID: 7479860
  49. Immunocytochemical identification of cone bipolar cells in the rat retina.
    J Comp Neurol. 1995 Oct 23;361(3):461-78 PMID: 8550893
  50. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings.
    J Neurosci. 1996 Jan 15;16(2):563-71 PMID: 8551340
Article Info
Journal
Neuron
Abbr.
Neuron
ISSN
0896-6273
Published
2002-11-14
Pages
703-12
Language
English
Region
United States
NLM ID
8809320
PMCID
PMC2834592
Subset
IM
Grants
NIGMS NIH HHS · R01 GM037751-20 · United States
NEI NIH HHS · R01 EY014127-03 · United States
NEI NIH HHS · R01 EY014127-01A2 · United States
NEI NIH HHS · R01 EY007360 · United States
NIGMS NIH HHS · R01 GM037751-23 · United States
NIGMS NIH HHS · R01 GM037751-18 · United States
NIGMS NIH HHS · R01 GM037751-21 · United States
NEI NIH HHS · R01 EY014127 · United States
NIGMS NIH HHS · R01 GM018974 · United States
NIGMS NIH HHS · R01 GM037751-17 · United States
NEI NIH HHS · R01 EY014127-04 · United States
NICHD NIH HHS · P30 HD018655 · United States
NIGMS NIH HHS · GM37751 · United States
NIGMS NIH HHS · R01 GM037751-22 · United States
NIGMS NIH HHS · R01 GM037751-15 · United States
NIGMS NIH HHS · GM18974 · United States
NIGMS NIH HHS · R01 GM037751-14 · United States
NIGMS NIH HHS · R01 GM037751-16 · United States
NEI NIH HHS · R01 EY014127-02 · United States
NEI NIH HHS · EY07360 · United States
NIGMS NIH HHS · R01 GM037751-19 · United States
NIGMS NIH HHS · R01 GM037751-13 · United States
NIGMS NIH HHS · R01 GM037751 · United States
NICHD NIH HHS · P30-HD18655 · 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]