DOI: 10.1038/nature09818. Wiring specificity in the direction-selectivity circuit of the retina

Wiring specificity in the direction-selectivity circuit of the retina

10.1038/nature09818

Crossref journal-article

Springer Science and Business Media LLC

Nature (297)

Bibliography

Briggman, K. L., Helmstaedter, M., & Denk, W. (2011). Wiring specificity in the direction-selectivity circuit of the retina. Nature, 471(7337), 183â188.

Authors 3

Kevin L. Briggman (first)
Moritz Helmstaedter (additional)
Winfried Denk (additional)

References 55 Referenced 774

Barlow, H. B., Hill, R. M. & Levick, W. R. Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. (Lond.) 173, 377–407 (1964) (10.1113/jphysiol.1964.sp007463) / J. Physiol. (Lond.) by HB Barlow (1964)
Barlow, H. B. & Levick, W. R. The mechanism of directionally selective units in rabbit’s retina. J. Physiol. (Lond.) 178, 477–504 (1965) (10.1113/jphysiol.1965.sp007638) / J. Physiol. (Lond.) by HB Barlow (1965)
Taylor, W. R. & Vaney, D. I. Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J. Neurosci. 22, 7712–7720 (2002) (10.1523/JNEUROSCI.22-17-07712.2002) / J. Neurosci. by WR Taylor (2002)
Fried, S. I., Munch, T. A. & Werblin, F. S. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411–414 (2002) (10.1038/nature01179) / Nature by SI Fried (2002)
Famiglietti, E. V. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J. Comp. Neurol. 309, 40–70 (1991) (10.1002/cne.903090105) / J. Comp. Neurol. by EV Famiglietti (1991)
Tauchi, M. & Masland, R. H. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc. R. Soc. Lond. B 223, 101–119 (1984) (10.1098/rspb.1984.0085) / Proc. R. Soc. Lond. B by M Tauchi (1984)
Yoshida, K. et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771–780 (2001) (10.1016/S0896-6273(01)00316-6) / Neuron by K Yoshida (2001)
O’Malley, D. M., Sandell, J. H. & Masland, R. H. Co-release of acetylcholine and GABA by the starburst amacrine cells. J. Neurosci. 12, 1394–1408 (1992) (10.1523/JNEUROSCI.12-04-01394.1992) / J. Neurosci. by DM O’Malley (1992)
Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845–852 (2002) (10.1038/nature00931) / Nature by T Euler (2002)
Chiao, C. C. & Masland, R. H. Starburst cells nondirectionally facilitate the responses of direction-selective retinal ganglion cells. J. Neurosci. 22, 10509–10513 (2002) (10.1523/JNEUROSCI.22-24-10509.2002) / J. Neurosci. by CC Chiao (2002)
Grzywacz, N. M., Tootle, J. S. & Amthor, F. R. Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit’s retinal directional selectivity? Vis. Neurosci. 14, 39–54 (1997) (10.1017/S0952523800008749) / Vis. Neurosci. by NM Grzywacz (1997)
Taylor, W. R. & Vaney, D. I. New directions in retinal research. Trends Neurosci. 26, 379–385 (2003) (10.1016/S0166-2236(03)00167-X) / Trends Neurosci. by WR Taylor (2003)
Demb, J. B. Cellular mechanisms for direction selectivity in the retina. Neuron 55, 179–186 (2007) (10.1016/j.neuron.2007.07.001) / Neuron by JB Demb (2007)
Schachter, M. J. et al. Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLOS Comput. Biol. 6, (2010) (10.1371/journal.pcbi.1000899)
Borg-Graham, L. J. The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neurosci. 4, 176–183 (2001) (10.1038/84007) / Nature Neurosci. by LJ Borg-Graham (2001)
Wei, W., Hamby, A. M., Zhou, K. & Feller, M. B. Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469, 402–406 (2010) (10.1038/nature09600) / Nature by W Wei (2010)
Lee, S., Kim, K. & Zhou, Z. J. Role of ACh-GABA co-transmission in detecting image motion and motion direction. Neuron 68, 1159–1172 (2010) (10.1016/j.neuron.2010.11.031) / Neuron by S Lee (2010)
Yonehara, K. et al. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469, 407–410 (2010) (10.1038/nature09711) / Nature by K Yonehara (2010)
Mumm, J. S. et al. Laminar circuit formation in the vertebrate retina. Prog. Brain Res. 147, 155–169 (2005) (10.1016/S0079-6123(04)47012-5) / Prog. Brain Res. by JS Mumm (2005)
Famiglietti, E. V. A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Vis. Neurosci. 19, 145–162 (2002) (10.1017/S0952523802191139) / Vis. Neurosci. by EV Famiglietti (2002)
Dong, W. et al. Dendritic relationship between starburst amacrine cells and direction-selective ganglion cells in the rabbit retina. J. Physiol. (Lond.) 556, 11–17 (2004) (10.1113/jphysiol.2004.060715) / J. Physiol. (Lond.) by W Dong (2004)
Chen, Y. C. & Chiao, C. C. Symmetric synaptic patterns between starburst amacrine cells and direction selective ganglion cells in the rabbit retina. J. Comp. Neurol. 508, 175–183 (2008) (10.1002/cne.21677) / J. Comp. Neurol. by YC Chen (2008)
Dacheux, R. F., Chimento, M. F. & Amthor, F. R. Synaptic input to the on-off directionally selective ganglion cell in the rabbit retina. J. Comp. Neurol. 456, 267–278 (2003) (10.1002/cne.10521) / J. Comp. Neurol. by RF Dacheux (2003)
White, J. G. et al. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. 314, 1–340 (1986) (10.1098/rstb.1986.0056) / Phil. Trans. R. Soc. Lond. by JG White (1986)
Denk, W. & Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329 (2004) (10.1371/journal.pbio.0020329) / PLoS Biol. by W Denk (2004)
Oyster, C. W., Amthor, F. R. & Takahashi, E. S. Dendritic architecture of ON-OFF direction-selective ganglion cells in the rabbit retina. Vision Res. 33, 579–608 (1993) (10.1016/0042-6989(93)90181-U) / Vision Res. by CW Oyster (1993)
Yang, G. & Masland, R. H. Receptive fields and dendritic structure of directionally selective retinal ganglion cells. J. Neurosci. 14, 5267–5280 (1994) (10.1523/JNEUROSCI.14-09-05267.1994) / J. Neurosci. by G Yang (1994)
Denk, W. & Detwiler, P. B. Optical recording of light-evoked calcium signals in the functionally intact retina. Proc. Natl Acad. Sci. USA 96, 7035–7040 (1999) (10.1073/pnas.96.12.7035) / Proc. Natl Acad. Sci. USA by W Denk (1999)
Blankenship, A. G. et al. Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron 62, 230–241 (2009) (10.1016/j.neuron.2009.03.015) / Neuron by AG Blankenship (2009)
Stosiek, C. et al. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl Acad. Sci. USA 100, 7319–7324 (2003) (10.1073/pnas.1232232100) / Proc. Natl Acad. Sci. USA by C Stosiek (2003)
Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73–76 (1990) (10.1126/science.2321027) / Science by W Denk (1990)
Euler, T. et al. Eyecup scope–optical recordings of light stimulus-evoked fluorescence signals in the retina. Pflugers Arch. 457, 1393–1414 (2009) (10.1007/s00424-008-0603-5) / Pflugers Arch. by T Euler (2009)
Oyster, C. W. & Barlow, H. B. Direction-selective units in rabbit retina: distribution of preferred directions. Science 155, 841–842 (1967) (10.1126/science.155.3764.841) / Science by CW Oyster (1967)
Yamada, E. S. et al. Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. J. Comp. Neurol. 461, 76–90 (2003) (10.1002/cne.10672) / J. Comp. Neurol. by ES Yamada (2003)
Keeley, P. W. et al. Dendritic spread and functional coverage of starburst amacrine cells. J. Comp. Neurol. 505, 539–546 (2007) (10.1002/cne.21518) / J. Comp. Neurol. by PW Keeley (2007)
Hausselt, S. E. et al. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol. 5, e185 (2007) (10.1371/journal.pbio.0050185) / PLoS Biol. by SE Hausselt (2007)
Lee, S. & Zhou, Z. J. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787–799 (2006) (10.1016/j.neuron.2006.08.007) / Neuron by S Lee (2006)
Oesch, N. W. & Taylor, W. R. Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLoS ONE 5, e12447 (2010) (10.1371/journal.pone.0012447) / PLoS ONE by NW Oesch (2010)
He, S., Jin, Z. F. & Masland, R. H. The nondiscriminating zone of directionally selective retinal ganglion cells: comparison with dendritic structure and implications for mechanism. J. Neurosci. 19, 8049–8056 (1999) (10.1523/JNEUROSCI.19-18-08049.1999) / J. Neurosci. by S He (1999)
Kittila, C. A. & Massey, S. C. Effect of ON pathway blockade on directional selectivity in the rabbit retina. J. Neurophysiol. 73, 703–712 (1995) (10.1152/jn.1995.73.2.703) / J. Neurophysiol. by CA Kittila (1995)
Caldwell, J. H., Daw, N. W. & Wyatt, H. J. Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J. Physiol. (Lond.) 276, 277–298 (1978) (10.1113/jphysiol.1978.sp012233) / J. Physiol. (Lond.) by JH Caldwell (1978)
Vaney, D. I. & Young, H. M. GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res. 438, 369–373 (1988) (10.1016/0006-8993(88)91366-2) / Brain Res. by DI Vaney (1988)
Fried, S. I., Munch, T. A. & Werblin, F. S. Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117–127 (2005) (10.1016/j.neuron.2005.02.007) / Neuron by SI Fried (2005)
Dmitrieva, N. A. et al. Identification of cholinoceptive glycinergic neurons in the mammalian retina. J. Comp. Neurol. 456, 167–175 (2003) (10.1002/cne.10520) / J. Comp. Neurol. by NA Dmitrieva (2003)
Dmitrieva, N. A., Strang, C. E. & Keyser, K. T. Expression of α7 nicotinic acetylcholine receptors by bipolar, amacrine, and ganglion cells of the rabbit retina. J. Histochem. Cytochem. 55, 461–476 (2007) (10.1369/jhc.6A7116.2006) / J. Histochem. Cytochem. by NA Dmitrieva (2007)
Wickersham, I. R. et al. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nature Methods 4, 47–49 (2007) (10.1038/nmeth999) / Nature Methods by IR Wickersham (2007)
Granstedt, A. E. et al. Fluorescence-based monitoring of in vivo neural activity using a circuit-tracing pseudorabies virus. PLoS ONE 4, e6923 (2009) (10.1371/journal.pone.0006923) / PLoS ONE by AE Granstedt (2009)
Briggman, K. L. & Euler, T. Bulk electroporation and population calcium imaging in the adult mammalian retina. J. Neurophysiol (in the press)
Schlichtenbrede, F. C. et al. Toxicity assessment of intravitreal triamcinolone and bevacizumab in a retinal explant mouse model using two-photon microscopy. Invest. Ophthalmol. Vis. Sci. 50, 5880–5887 (2009) (10.1167/iovs.08-3078) / Invest. Ophthalmol. Vis. Sci. by FC Schlichtenbrede (2009)
Fahmy, A. An Extemporaneous Lead Citrate Stain for Electron Microscopy 148–149 (Proc. 25th Annu. EMSA Meeting, 1967) / An Extemporaneous Lead Citrate Stain for Electron Microscopy by A Fahmy (1967)
Glauert, A. M. & Lewis, P. R. Biological specimen preparation for transmission electron microscopy. In Practical Methods in Electron Microscopy xxi (Princeton Univ. Press, 1998) / Practical Methods in Electron Microscopy by AM Glauert (1998)
Karnovsky, M. J. Use of Ferrocyanide-reduced osmium in electron microscopy 146 (Proc. 14th Annual Meeting Am. Soc. Cell Biol., 1971) / Use of Ferrocyanide-reduced osmium in electron microscopy by MJ Karnovsky (1971)
Seligman, A. M., Wasserkrug, H. L. & Hanker, J. S. A new staining method (OTO) for enhancing contrast of lipid-containing membranes and droplets in osmium tetroxide-fixed tissue with osmiophilic thiocarbohydrazide (TCH). J. Cell Biol. 30, 424–432 (1966) (10.1083/jcb.30.2.424) / J. Cell Biol. by AM Seligman (1966)
Walton, J. Lead asparate, an en bloc contrast stain particularly useful for ultrastructural enzymology. J. Histochem. Cytochem. 27, 1337–1342 (1979) (10.1177/27.10.512319) / J. Histochem. Cytochem. by J Walton (1979)
Yushkevich, P. A. et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31, 1116–1128 (2006) (10.1016/j.neuroimage.2006.01.015) / Neuroimage by PA Yushkevich (2006)

Dates

Type	When
Created	14 years, 5 months ago (March 8, 2011, 9:57 a.m.)
Deposited	2 years, 3 months ago (May 18, 2023, 1:50 p.m.)
Indexed	14 minutes ago (Aug. 28, 2025, 2:21 p.m.)
Issued	14 years, 5 months ago (March 1, 2011)
Published	14 years, 5 months ago (March 1, 2011)
Published Online	14 years, 5 months ago (March 9, 2011)
Published Print	14 years, 5 months ago (March 1, 2011)

Funders 0

None

BibTeX

@article{Briggman_2011, title={Wiring specificity in the direction-selectivity circuit of the retina}, volume={471}, ISSN={1476-4687}, url={http://dx.doi.org/10.1038/nature09818}, DOI={10.1038/nature09818}, number={7337}, journal={Nature}, publisher={Springer Science and Business Media LLC}, author={Briggman, Kevin L. and Helmstaedter, Moritz and Denk, Winfried}, year={2011}, month=mar, pages={183–188} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        8,
        28
      ]
    ],
    "date-time": "2025-08-28T18:21:51Z",
    "timestamp": 1756405311198
  },
  "reference-count": 55,
  "publisher": "Springer Science and Business Media LLC",
  "issue": "7337",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2011,
            3,
            1
          ]
        ],
        "date-time": "2011-03-01T00:00:00Z",
        "timestamp": 1298937600000
      },
      "content-version": "tdm",
      "delay-in-days": 0,
      "URL": "http://www.springer.com/tdm"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2011,
        3
      ]
    ]
  },
  "DOI": "10.1038/nature09818",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2011,
        3,
        8
      ]
    ],
    "date-time": "2011-03-08T14:57:42Z",
    "timestamp": 1299596262000
  },
  "page": "183-188",
  "source": "Crossref",
  "is-referenced-by-count": 774,
  "title": "Wiring specificity in the direction-selectivity circuit of the retina",
  "prefix": "10.1038",
  "volume": "471",
  "author": [
    {
      "given": "Kevin L.",
      "family": "Briggman",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "Moritz",
      "family": "Helmstaedter",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Winfried",
      "family": "Denk",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "297",
  "published-online": {
    "date-parts": [
      [
        2011,
        3,
        9
      ]
    ]
  },
  "reference": [
    {
      "key": "BFnature09818_CR1",
      "doi-asserted-by": "publisher",
      "first-page": "377",
      "DOI": "10.1113/jphysiol.1964.sp007463",
      "volume": "173",
      "author": "HB Barlow",
      "year": "1964",
      "unstructured": "Barlow, H. B., Hill, R. M. & Levick, W. R. Retinal ganglion cells responding selectively to direction and speed of image motion in the rabbit. J. Physiol. (Lond.) 173, 377\u2013407 (1964)",
      "journal-title": "J. Physiol. (Lond.)"
    },
    {
      "key": "BFnature09818_CR2",
      "doi-asserted-by": "publisher",
      "first-page": "477",
      "DOI": "10.1113/jphysiol.1965.sp007638",
      "volume": "178",
      "author": "HB Barlow",
      "year": "1965",
      "unstructured": "Barlow, H. B. & Levick, W. R. The mechanism of directionally selective units in rabbit\u2019s retina. J. Physiol. (Lond.) 178, 477\u2013504 (1965)",
      "journal-title": "J. Physiol. (Lond.)"
    },
    {
      "key": "BFnature09818_CR3",
      "doi-asserted-by": "publisher",
      "first-page": "7712",
      "DOI": "10.1523/JNEUROSCI.22-17-07712.2002",
      "volume": "22",
      "author": "WR Taylor",
      "year": "2002",
      "unstructured": "Taylor, W. R. & Vaney, D. I. Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. J. Neurosci. 22, 7712\u20137720 (2002)",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "BFnature09818_CR4",
      "doi-asserted-by": "publisher",
      "first-page": "411",
      "DOI": "10.1038/nature01179",
      "volume": "420",
      "author": "SI Fried",
      "year": "2002",
      "unstructured": "Fried, S. I., Munch, T. A. & Werblin, F. S. Mechanisms and circuitry underlying directional selectivity in the retina. Nature 420, 411\u2013414 (2002)",
      "journal-title": "Nature"
    },
    {
      "key": "BFnature09818_CR5",
      "doi-asserted-by": "publisher",
      "first-page": "40",
      "DOI": "10.1002/cne.903090105",
      "volume": "309",
      "author": "EV Famiglietti",
      "year": "1991",
      "unstructured": "Famiglietti, E. V. Synaptic organization of starburst amacrine cells in rabbit retina: analysis of serial thin sections by electron microscopy and graphic reconstruction. J. Comp. Neurol. 309, 40\u201370 (1991)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR6",
      "doi-asserted-by": "publisher",
      "first-page": "101",
      "DOI": "10.1098/rspb.1984.0085",
      "volume": "223",
      "author": "M Tauchi",
      "year": "1984",
      "unstructured": "Tauchi, M. & Masland, R. H. The shape and arrangement of the cholinergic neurons in the rabbit retina. Proc. R. Soc. Lond. B 223, 101\u2013119 (1984)",
      "journal-title": "Proc. R. Soc. Lond. B"
    },
    {
      "key": "BFnature09818_CR7",
      "doi-asserted-by": "publisher",
      "first-page": "771",
      "DOI": "10.1016/S0896-6273(01)00316-6",
      "volume": "30",
      "author": "K Yoshida",
      "year": "2001",
      "unstructured": "Yoshida, K. et al. A key role of starburst amacrine cells in originating retinal directional selectivity and optokinetic eye movement. Neuron 30, 771\u2013780 (2001)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR8",
      "doi-asserted-by": "publisher",
      "first-page": "1394",
      "DOI": "10.1523/JNEUROSCI.12-04-01394.1992",
      "volume": "12",
      "author": "DM O\u2019Malley",
      "year": "1992",
      "unstructured": "O\u2019Malley, D. M., Sandell, J. H. & Masland, R. H. Co-release of acetylcholine and GABA by the starburst amacrine cells. J. Neurosci. 12, 1394\u20131408 (1992)",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "BFnature09818_CR9",
      "doi-asserted-by": "publisher",
      "first-page": "845",
      "DOI": "10.1038/nature00931",
      "volume": "418",
      "author": "T Euler",
      "year": "2002",
      "unstructured": "Euler, T., Detwiler, P. B. & Denk, W. Directionally selective calcium signals in dendrites of starburst amacrine cells. Nature 418, 845\u2013852 (2002)",
      "journal-title": "Nature"
    },
    {
      "key": "BFnature09818_CR10",
      "doi-asserted-by": "publisher",
      "first-page": "10509",
      "DOI": "10.1523/JNEUROSCI.22-24-10509.2002",
      "volume": "22",
      "author": "CC Chiao",
      "year": "2002",
      "unstructured": "Chiao, C. C. & Masland, R. H. Starburst cells nondirectionally facilitate the responses of direction-selective retinal ganglion cells. J. Neurosci. 22, 10509\u201310513 (2002)",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "BFnature09818_CR11",
      "doi-asserted-by": "publisher",
      "first-page": "39",
      "DOI": "10.1017/S0952523800008749",
      "volume": "14",
      "author": "NM Grzywacz",
      "year": "1997",
      "unstructured": "Grzywacz, N. M., Tootle, J. S. & Amthor, F. R. Is the input to a GABAergic or cholinergic synapse the sole asymmetry in rabbit\u2019s retinal directional selectivity? Vis. Neurosci. 14, 39\u201354 (1997)",
      "journal-title": "Vis. Neurosci."
    },
    {
      "key": "BFnature09818_CR12",
      "doi-asserted-by": "publisher",
      "first-page": "379",
      "DOI": "10.1016/S0166-2236(03)00167-X",
      "volume": "26",
      "author": "WR Taylor",
      "year": "2003",
      "unstructured": "Taylor, W. R. & Vaney, D. I. New directions in retinal research. Trends Neurosci. 26, 379\u2013385 (2003)",
      "journal-title": "Trends Neurosci."
    },
    {
      "key": "BFnature09818_CR13",
      "doi-asserted-by": "publisher",
      "first-page": "179",
      "DOI": "10.1016/j.neuron.2007.07.001",
      "volume": "55",
      "author": "JB Demb",
      "year": "2007",
      "unstructured": "Demb, J. B. Cellular mechanisms for direction selectivity in the retina. Neuron 55, 179\u2013186 (2007)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR14",
      "doi-asserted-by": "crossref",
      "unstructured": "Schachter, M. J. et al. Dendritic spikes amplify the synaptic signal to enhance detection of motion in a simulation of the direction-selective ganglion cell. PLOS Comput. Biol. 6, (2010)",
      "DOI": "10.1371/journal.pcbi.1000899"
    },
    {
      "key": "BFnature09818_CR15",
      "doi-asserted-by": "publisher",
      "first-page": "176",
      "DOI": "10.1038/84007",
      "volume": "4",
      "author": "LJ Borg-Graham",
      "year": "2001",
      "unstructured": "Borg-Graham, L. J. The computation of directional selectivity in the retina occurs presynaptic to the ganglion cell. Nature Neurosci. 4, 176\u2013183 (2001)",
      "journal-title": "Nature Neurosci."
    },
    {
      "key": "BFnature09818_CR16",
      "doi-asserted-by": "publisher",
      "first-page": "402",
      "DOI": "10.1038/nature09600",
      "volume": "469",
      "author": "W Wei",
      "year": "2010",
      "unstructured": "Wei, W., Hamby, A. M., Zhou, K. & Feller, M. B. Development of asymmetric inhibition underlying direction selectivity in the retina. Nature 469, 402\u2013406 (2010)",
      "journal-title": "Nature"
    },
    {
      "key": "BFnature09818_CR17",
      "doi-asserted-by": "publisher",
      "first-page": "1159",
      "DOI": "10.1016/j.neuron.2010.11.031",
      "volume": "68",
      "author": "S Lee",
      "year": "2010",
      "unstructured": "Lee, S., Kim, K. & Zhou, Z. J. Role of ACh-GABA co-transmission in detecting image motion and motion direction. Neuron 68, 1159\u20131172 (2010)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR18",
      "doi-asserted-by": "publisher",
      "first-page": "407",
      "DOI": "10.1038/nature09711",
      "volume": "469",
      "author": "K Yonehara",
      "year": "2010",
      "unstructured": "Yonehara, K. et al. Spatially asymmetric reorganization of inhibition establishes a motion-sensitive circuit. Nature 469, 407\u2013410 (2010)",
      "journal-title": "Nature"
    },
    {
      "key": "BFnature09818_CR19",
      "doi-asserted-by": "publisher",
      "first-page": "155",
      "DOI": "10.1016/S0079-6123(04)47012-5",
      "volume": "147",
      "author": "JS Mumm",
      "year": "2005",
      "unstructured": "Mumm, J. S. et al. Laminar circuit formation in the vertebrate retina. Prog. Brain Res. 147, 155\u2013169 (2005)",
      "journal-title": "Prog. Brain Res."
    },
    {
      "key": "BFnature09818_CR20",
      "doi-asserted-by": "publisher",
      "first-page": "145",
      "DOI": "10.1017/S0952523802191139",
      "volume": "19",
      "author": "EV Famiglietti",
      "year": "2002",
      "unstructured": "Famiglietti, E. V. A structural basis for omnidirectional connections between starburst amacrine cells and directionally selective ganglion cells in rabbit retina, with associated bipolar cells. Vis. Neurosci. 19, 145\u2013162 (2002)",
      "journal-title": "Vis. Neurosci."
    },
    {
      "key": "BFnature09818_CR21",
      "doi-asserted-by": "publisher",
      "first-page": "11",
      "DOI": "10.1113/jphysiol.2004.060715",
      "volume": "556",
      "author": "W Dong",
      "year": "2004",
      "unstructured": "Dong, W. et al. Dendritic relationship between starburst amacrine cells and direction-selective ganglion cells in the rabbit retina. J. Physiol. (Lond.) 556, 11\u201317 (2004)",
      "journal-title": "J. Physiol. (Lond.)"
    },
    {
      "key": "BFnature09818_CR22",
      "doi-asserted-by": "publisher",
      "first-page": "175",
      "DOI": "10.1002/cne.21677",
      "volume": "508",
      "author": "YC Chen",
      "year": "2008",
      "unstructured": "Chen, Y. C. & Chiao, C. C. Symmetric synaptic patterns between starburst amacrine cells and direction selective ganglion cells in the rabbit retina. J. Comp. Neurol. 508, 175\u2013183 (2008)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR23",
      "doi-asserted-by": "publisher",
      "first-page": "267",
      "DOI": "10.1002/cne.10521",
      "volume": "456",
      "author": "RF Dacheux",
      "year": "2003",
      "unstructured": "Dacheux, R. F., Chimento, M. F. & Amthor, F. R. Synaptic input to the on-off directionally selective ganglion cell in the rabbit retina. J. Comp. Neurol. 456, 267\u2013278 (2003)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR24",
      "doi-asserted-by": "publisher",
      "first-page": "1",
      "DOI": "10.1098/rstb.1986.0056",
      "volume": "314",
      "author": "JG White",
      "year": "1986",
      "unstructured": "White, J. G. et al. The structure of the nervous system of the nematode Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. 314, 1\u2013340 (1986)",
      "journal-title": "Phil. Trans. R. Soc. Lond."
    },
    {
      "key": "BFnature09818_CR25",
      "doi-asserted-by": "publisher",
      "first-page": "e329",
      "DOI": "10.1371/journal.pbio.0020329",
      "volume": "2",
      "author": "W Denk",
      "year": "2004",
      "unstructured": "Denk, W. & Horstmann, H. Serial block-face scanning electron microscopy to reconstruct three-dimensional tissue nanostructure. PLoS Biol. 2, e329 (2004)",
      "journal-title": "PLoS Biol."
    },
    {
      "key": "BFnature09818_CR26",
      "doi-asserted-by": "publisher",
      "first-page": "579",
      "DOI": "10.1016/0042-6989(93)90181-U",
      "volume": "33",
      "author": "CW Oyster",
      "year": "1993",
      "unstructured": "Oyster, C. W., Amthor, F. R. & Takahashi, E. S. Dendritic architecture of ON-OFF direction-selective ganglion cells in the rabbit retina. Vision Res. 33, 579\u2013608 (1993)",
      "journal-title": "Vision Res."
    },
    {
      "key": "BFnature09818_CR27",
      "doi-asserted-by": "publisher",
      "first-page": "5267",
      "DOI": "10.1523/JNEUROSCI.14-09-05267.1994",
      "volume": "14",
      "author": "G Yang",
      "year": "1994",
      "unstructured": "Yang, G. & Masland, R. H. Receptive fields and dendritic structure of directionally selective retinal ganglion cells. J. Neurosci. 14, 5267\u20135280 (1994)",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "BFnature09818_CR28",
      "doi-asserted-by": "publisher",
      "first-page": "7035",
      "DOI": "10.1073/pnas.96.12.7035",
      "volume": "96",
      "author": "W Denk",
      "year": "1999",
      "unstructured": "Denk, W. & Detwiler, P. B. Optical recording of light-evoked calcium signals in the functionally intact retina. Proc. Natl Acad. Sci. USA 96, 7035\u20137040 (1999)",
      "journal-title": "Proc. Natl Acad. Sci. USA"
    },
    {
      "key": "BFnature09818_CR29",
      "doi-asserted-by": "publisher",
      "first-page": "230",
      "DOI": "10.1016/j.neuron.2009.03.015",
      "volume": "62",
      "author": "AG Blankenship",
      "year": "2009",
      "unstructured": "Blankenship, A. G. et al. Synaptic and extrasynaptic factors governing glutamatergic retinal waves. Neuron 62, 230\u2013241 (2009)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR30",
      "doi-asserted-by": "publisher",
      "first-page": "7319",
      "DOI": "10.1073/pnas.1232232100",
      "volume": "100",
      "author": "C Stosiek",
      "year": "2003",
      "unstructured": "Stosiek, C. et al. In vivo two-photon calcium imaging of neuronal networks. Proc. Natl Acad. Sci. USA 100, 7319\u20137324 (2003)",
      "journal-title": "Proc. Natl Acad. Sci. USA"
    },
    {
      "key": "BFnature09818_CR31",
      "doi-asserted-by": "publisher",
      "first-page": "73",
      "DOI": "10.1126/science.2321027",
      "volume": "248",
      "author": "W Denk",
      "year": "1990",
      "unstructured": "Denk, W., Strickler, J. H. & Webb, W. W. Two-photon laser scanning fluorescence microscopy. Science 248, 73\u201376 (1990)",
      "journal-title": "Science"
    },
    {
      "key": "BFnature09818_CR32",
      "doi-asserted-by": "publisher",
      "first-page": "1393",
      "DOI": "10.1007/s00424-008-0603-5",
      "volume": "457",
      "author": "T Euler",
      "year": "2009",
      "unstructured": "Euler, T. et al. Eyecup scope\u2013optical recordings of light stimulus-evoked fluorescence signals in the retina. Pflugers Arch. 457, 1393\u20131414 (2009)",
      "journal-title": "Pflugers Arch."
    },
    {
      "key": "BFnature09818_CR33",
      "doi-asserted-by": "publisher",
      "first-page": "841",
      "DOI": "10.1126/science.155.3764.841",
      "volume": "155",
      "author": "CW Oyster",
      "year": "1967",
      "unstructured": "Oyster, C. W. & Barlow, H. B. Direction-selective units in rabbit retina: distribution of preferred directions. Science 155, 841\u2013842 (1967)",
      "journal-title": "Science"
    },
    {
      "key": "BFnature09818_CR34",
      "doi-asserted-by": "publisher",
      "first-page": "76",
      "DOI": "10.1002/cne.10672",
      "volume": "461",
      "author": "ES Yamada",
      "year": "2003",
      "unstructured": "Yamada, E. S. et al. Synaptic connections of starburst amacrine cells and localization of acetylcholine receptors in primate retinas. J. Comp. Neurol. 461, 76\u201390 (2003)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR35",
      "doi-asserted-by": "publisher",
      "first-page": "539",
      "DOI": "10.1002/cne.21518",
      "volume": "505",
      "author": "PW Keeley",
      "year": "2007",
      "unstructured": "Keeley, P. W. et al. Dendritic spread and functional coverage of starburst amacrine cells. J. Comp. Neurol. 505, 539\u2013546 (2007)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR36",
      "doi-asserted-by": "publisher",
      "first-page": "e185",
      "DOI": "10.1371/journal.pbio.0050185",
      "volume": "5",
      "author": "SE Hausselt",
      "year": "2007",
      "unstructured": "Hausselt, S. E. et al. A dendrite-autonomous mechanism for direction selectivity in retinal starburst amacrine cells. PLoS Biol. 5, e185 (2007)",
      "journal-title": "PLoS Biol."
    },
    {
      "key": "BFnature09818_CR37",
      "doi-asserted-by": "publisher",
      "first-page": "787",
      "DOI": "10.1016/j.neuron.2006.08.007",
      "volume": "51",
      "author": "S Lee",
      "year": "2006",
      "unstructured": "Lee, S. & Zhou, Z. J. The synaptic mechanism of direction selectivity in distal processes of starburst amacrine cells. Neuron 51, 787\u2013799 (2006)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR38",
      "doi-asserted-by": "publisher",
      "first-page": "e12447",
      "DOI": "10.1371/journal.pone.0012447",
      "volume": "5",
      "author": "NW Oesch",
      "year": "2010",
      "unstructured": "Oesch, N. W. & Taylor, W. R. Tetrodotoxin-resistant sodium channels contribute to directional responses in starburst amacrine cells. PLoS ONE 5, e12447 (2010)",
      "journal-title": "PLoS ONE"
    },
    {
      "key": "BFnature09818_CR39",
      "doi-asserted-by": "publisher",
      "first-page": "8049",
      "DOI": "10.1523/JNEUROSCI.19-18-08049.1999",
      "volume": "19",
      "author": "S He",
      "year": "1999",
      "unstructured": "He, S., Jin, Z. F. & Masland, R. H. The nondiscriminating zone of directionally selective retinal ganglion cells: comparison with dendritic structure and implications for mechanism. J. Neurosci. 19, 8049\u20138056 (1999)",
      "journal-title": "J. Neurosci."
    },
    {
      "key": "BFnature09818_CR40",
      "doi-asserted-by": "publisher",
      "first-page": "703",
      "DOI": "10.1152/jn.1995.73.2.703",
      "volume": "73",
      "author": "CA Kittila",
      "year": "1995",
      "unstructured": "Kittila, C. A. & Massey, S. C. Effect of ON pathway blockade on directional selectivity in the rabbit retina. J. Neurophysiol. 73, 703\u2013712 (1995)",
      "journal-title": "J. Neurophysiol."
    },
    {
      "key": "BFnature09818_CR41",
      "doi-asserted-by": "publisher",
      "first-page": "277",
      "DOI": "10.1113/jphysiol.1978.sp012233",
      "volume": "276",
      "author": "JH Caldwell",
      "year": "1978",
      "unstructured": "Caldwell, J. H., Daw, N. W. & Wyatt, H. J. Effects of picrotoxin and strychnine on rabbit retinal ganglion cells: lateral interactions for cells with more complex receptive fields. J. Physiol. (Lond.) 276, 277\u2013298 (1978)",
      "journal-title": "J. Physiol. (Lond.)"
    },
    {
      "key": "BFnature09818_CR42",
      "doi-asserted-by": "publisher",
      "first-page": "369",
      "DOI": "10.1016/0006-8993(88)91366-2",
      "volume": "438",
      "author": "DI Vaney",
      "year": "1988",
      "unstructured": "Vaney, D. I. & Young, H. M. GABA-like immunoreactivity in cholinergic amacrine cells of the rabbit retina. Brain Res. 438, 369\u2013373 (1988)",
      "journal-title": "Brain Res."
    },
    {
      "key": "BFnature09818_CR43",
      "doi-asserted-by": "publisher",
      "first-page": "117",
      "DOI": "10.1016/j.neuron.2005.02.007",
      "volume": "46",
      "author": "SI Fried",
      "year": "2005",
      "unstructured": "Fried, S. I., Munch, T. A. & Werblin, F. S. Directional selectivity is formed at multiple levels by laterally offset inhibition in the rabbit retina. Neuron 46, 117\u2013127 (2005)",
      "journal-title": "Neuron"
    },
    {
      "key": "BFnature09818_CR44",
      "doi-asserted-by": "publisher",
      "first-page": "167",
      "DOI": "10.1002/cne.10520",
      "volume": "456",
      "author": "NA Dmitrieva",
      "year": "2003",
      "unstructured": "Dmitrieva, N. A. et al. Identification of cholinoceptive glycinergic neurons in the mammalian retina. J. Comp. Neurol. 456, 167\u2013175 (2003)",
      "journal-title": "J. Comp. Neurol."
    },
    {
      "key": "BFnature09818_CR45",
      "doi-asserted-by": "publisher",
      "first-page": "461",
      "DOI": "10.1369/jhc.6A7116.2006",
      "volume": "55",
      "author": "NA Dmitrieva",
      "year": "2007",
      "unstructured": "Dmitrieva, N. A., Strang, C. E. & Keyser, K. T. Expression of \u03b17 nicotinic acetylcholine receptors by bipolar, amacrine, and ganglion cells of the rabbit retina. J. Histochem. Cytochem. 55, 461\u2013476 (2007)",
      "journal-title": "J. Histochem. Cytochem."
    },
    {
      "key": "BFnature09818_CR46",
      "doi-asserted-by": "publisher",
      "first-page": "47",
      "DOI": "10.1038/nmeth999",
      "volume": "4",
      "author": "IR Wickersham",
      "year": "2007",
      "unstructured": "Wickersham, I. R. et al. Retrograde neuronal tracing with a deletion-mutant rabies virus. Nature Methods 4, 47\u201349 (2007)",
      "journal-title": "Nature Methods"
    },
    {
      "key": "BFnature09818_CR47",
      "doi-asserted-by": "publisher",
      "first-page": "e6923",
      "DOI": "10.1371/journal.pone.0006923",
      "volume": "4",
      "author": "AE Granstedt",
      "year": "2009",
      "unstructured": "Granstedt, A. E. et al. Fluorescence-based monitoring of in vivo neural activity using a circuit-tracing pseudorabies virus. PLoS ONE 4, e6923 (2009)",
      "journal-title": "PLoS ONE"
    },
    {
      "key": "BFnature09818_CR48",
      "unstructured": "Briggman, K. L. & Euler, T. Bulk electroporation and population calcium imaging in the adult mammalian retina. J. Neurophysiol (in the press)"
    },
    {
      "key": "BFnature09818_CR49",
      "doi-asserted-by": "publisher",
      "first-page": "5880",
      "DOI": "10.1167/iovs.08-3078",
      "volume": "50",
      "author": "FC Schlichtenbrede",
      "year": "2009",
      "unstructured": "Schlichtenbrede, F. C. et al. Toxicity assessment of intravitreal triamcinolone and bevacizumab in a retinal explant mouse model using two-photon microscopy. Invest. Ophthalmol. Vis. Sci. 50, 5880\u20135887 (2009)",
      "journal-title": "Invest. Ophthalmol. Vis. Sci."
    },
    {
      "key": "BFnature09818_CR50",
      "first-page": "148",
      "volume-title": "An Extemporaneous Lead Citrate Stain for Electron Microscopy",
      "author": "A Fahmy",
      "year": "1967",
      "unstructured": "Fahmy, A. An Extemporaneous Lead Citrate Stain for Electron Microscopy 148\u2013149 (Proc. 25th Annu. EMSA Meeting, 1967)"
    },
    {
      "key": "BFnature09818_CR51",
      "first-page": "xxi",
      "volume-title": "Practical Methods in Electron Microscopy",
      "author": "AM Glauert",
      "year": "1998",
      "unstructured": "Glauert, A. M. & Lewis, P. R. Biological specimen preparation for transmission electron microscopy. In Practical Methods in Electron Microscopy xxi (Princeton Univ. Press, 1998)"
    },
    {
      "key": "BFnature09818_CR52",
      "first-page": "146",
      "volume-title": "Use of Ferrocyanide-reduced osmium in electron microscopy",
      "author": "MJ Karnovsky",
      "year": "1971",
      "unstructured": "Karnovsky, M. J. Use of Ferrocyanide-reduced osmium in electron microscopy 146 (Proc. 14th Annual Meeting Am. Soc. Cell Biol., 1971)"
    },
    {
      "key": "BFnature09818_CR53",
      "doi-asserted-by": "publisher",
      "first-page": "424",
      "DOI": "10.1083/jcb.30.2.424",
      "volume": "30",
      "author": "AM Seligman",
      "year": "1966",
      "unstructured": "Seligman, A. M., Wasserkrug, H. L. & Hanker, J. S. A new staining method (OTO) for enhancing contrast of lipid-containing membranes and droplets in osmium tetroxide-fixed tissue with osmiophilic thiocarbohydrazide (TCH). J. Cell Biol. 30, 424\u2013432 (1966)",
      "journal-title": "J. Cell Biol."
    },
    {
      "key": "BFnature09818_CR54",
      "doi-asserted-by": "publisher",
      "first-page": "1337",
      "DOI": "10.1177/27.10.512319",
      "volume": "27",
      "author": "J Walton",
      "year": "1979",
      "unstructured": "Walton, J. Lead asparate, an en bloc contrast stain particularly useful for ultrastructural enzymology. J. Histochem. Cytochem. 27, 1337\u20131342 (1979)",
      "journal-title": "J. Histochem. Cytochem."
    },
    {
      "key": "BFnature09818_CR55",
      "doi-asserted-by": "publisher",
      "first-page": "1116",
      "DOI": "10.1016/j.neuroimage.2006.01.015",
      "volume": "31",
      "author": "PA Yushkevich",
      "year": "2006",
      "unstructured": "Yushkevich, P. A. et al. User-guided 3D active contour segmentation of anatomical structures: significantly improved efficiency and reliability. Neuroimage 31, 1116\u20131128 (2006)",
      "journal-title": "Neuroimage"
    }
  ],
  "container-title": "Nature",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "http://www.nature.com/articles/nature09818.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "http://www.nature.com/articles/nature09818",
      "content-type": "text/html",
      "content-version": "vor",
      "intended-application": "text-mining"
    },
    {
      "URL": "http://www.nature.com/articles/nature09818.pdf",
      "content-type": "application/pdf",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        5,
        18
      ]
    ],
    "date-time": "2023-05-18T17:50:36Z",
    "timestamp": 1684432236000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.nature.com/articles/nature09818"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2011,
        3
      ]
    ]
  },
  "references-count": 55,
  "journal-issue": {
    "issue": "7337",
    "published-print": {
      "date-parts": [
        [
          2011,
          3
        ]
      ]
    }
  },
  "alternative-id": [
    "BFnature09818"
  ],
  "URL": "http://dx.doi.org/10.1038/nature09818",
  "relation": {
    "has-review": [
      {
        "id-type": "doi",
        "id": "10.3410/f.9492959.10139059",
        "asserted-by": "object"
      }
    ]
  },
  "ISSN": [
    "0028-0836",
    "1476-4687"
  ],
  "subject": [],
  "container-title-short": "Nature",
  "published": {
    "date-parts": [
      [
        2011,
        3
      ]
    ]
  }
}