Interacting linear and nonlinear characteristics produce population coding asymmetries between ON and OFF cells in the retina

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14958-14973

  Nichols, Zachary ^a   Nirenberg, Sheila ^a   Victor, Jonathan ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DARK ADAPTATION; ELECTROPHYSIOLOGY; FEMALE; LATENT PERIOD; LIGHT ADAPTATION; MATHEMATICAL MODEL; MOTION; MOUSE; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RESPONSE TIME; RETINA GANGLION CELL; RETINA RECEPTIVE FIELD; SPATIOTEMPORAL ANALYSIS; SPIKE WAVE; TASK PERFORMANCE; VISUAL DISCRIMINATION; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; DISCRIMINATION (PSYCHOLOGY); LIGHT; LINEAR MODELS; MICE; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; MOTION PERCEPTION; NEURAL PATHWAYS; NONLINEAR DYNAMICS; PHOTIC STIMULATION; RETINA; RETINAL GANGLION CELLS;

EID: 84883710471     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1004-13.2013     Document Type: Article

References (55)

1. Applebury ML, Antoch MP, Baxter LC, Chun LL, Falk JD, Farhangfar F, Kage K, Krzystolik MG, Lyass LA, Robbins JT (2000) The murine cone photoreceptor: a single cone type expresses both S and M opsins with retinal spatial patterning. Neuron 27:513-523. CrossRef Medline
2. Balasubramanian V, Sterling P (2009) Receptive fields and functional architecture in the retina. J Physiol 587:2753-2767. CrossRef Medline
3. Bomash I, Roudi Y, Nirenberg S (2013) The virtual retina. PLoS One 8:e53363. CrossRef Medline
4. Bowen RW, Pokorny J, Smith VC (1989) Sawtooth contrast sensitivity: decrements have the edge. Vision Res 29:1501-1509. Medline
5. Britten KH, Shadlen MN, Newsome WT, Movshon JA (1992) The analysis of visual motion: a comparison of neuronal and psychophysical performance. J Neurosci 12:4745-4765. Medline
6. Buchner A, Baumgartner N (2007) Text-background polarity affects performance irrespective of ambient illumination and colour contrast. Ergonomics 50:1036-1063. CrossRef Medline
7. Burkhardt DA (2011) Contrast processing byONand OFF bipolar cells. Vis Neurosci 28:69-75. CrossRef Medline
8. Burkhardt DA, Fahey PK, Sikora M (1998) Responses of ganglion cells to contrast steps in the light-adapted retina of the tiger salamander. Vis Neurosci 15:219-229. Medline
9. Cai D, DeAngelis GC, Freeman RD (1997) Spatiotemporal receptive field organization in the lateral geniculate nucleus of cats and kittens. J Neurophysiol 78:1045-1061. Medline
10. Calabrese A, Schumacher JW, Schneider DM, Paninski L, Woolley SM (2011) A generalized linear model for estimating spectrotemporal receptive fields from responses to natural sounds. PLoS One 6:e16104. CrossRef Medline
11. Carcieri SM, Jacobs AL, Nirenberg S (2003) Classification of retinal ganglion cells: a statistical approach. J Neurophysiol 90:1704-1713. CrossRef Medline
12. Chacron MJ (2006) Nonlinear information processing in a model sensory system. J Neurophysiol 95:2933-2946. CrossRef Medline
13. Chichilnisky EJ, Kalmar RS (2002) Functional asymmetries in ON and OFF ganglion cells of primate retina. J Neurosci 22:2737-2747. Medline
14. Dowling JE, Ripps H (1970) Visual adaptation in the retina of the skate. J Gen Physiol 56:491-520. CrossRef Medline
15. Dryja TP, McGee TL, Berson EL, Fishman GA, Sandberg MA, Alexander KR, Derlacki DJ, Rajagopalan AS (2005) Night blindess and abnormal cone electroretinogram ON responses in patients with mutations in the GRM6 gene encoding mGluR6. Proc Natl Acad Sci U S A 102:4884-4889. CrossRef Medline
16. Fee MS, Mitra PP, Kleinfeld D (1996) Automatic sorting of multiple unit neuronal signals in the presence of anisotropic and non-Gaussian variability. J Neurosci Methods 69:175-188. CrossRef Medline
17. Gollisch T, Meister M (2008) Modeling convergent ON and OFF pathways in the early visual system. Biol Cybern 99:263-278. CrossRef Medline
18. Grzywacz NM, Amthor FR (2007) Robust directional computation in onoff directionally selective ganglion cells of rabbit retina. Vis Neurosci 24:647-661. Medline
19. Hartline HK (1938) The response of single optic nerve fibers of the vertebrate eye to illumination of the retina. Am J Physiol 121:400-415.
20. Jacobs AL, Fridman G, Douglas RM, Alam NM, Latham PE, Prusky GT, Nirenberg S (2009) Ruling out and ruling in neural codes. Proc Natl Acad Sci U S A 106:5936-5941. CrossRef Medline
21. Jeon CJ, Strettoi E, Masland RH (1998) The major populations of the mouse retina. J Neurosci 18:8936-8946. Medline
22. Jin J, Wang Y, Swadlow HA, Alonso JM (2011a) Population receptive fields ofONand OFF thalamic inputs to an orientation column in visual cortex. Nat Neurosci 14:232-238. CrossRef Medline
23. Jin J, Wang Y, Lashgari R, Swadlow HA, Alonso JM (2011b) Faster thalamocortical processing for dark than light visual targets. J Neurosci 31:17471-17479. CrossRef Medline
24. Jin JZ, Weng C, Yeh CI, Gordon JA, Ruthazer ES, Stryker MP, Swadlow HA, Alonso JM (2008) On and off domains of geniculate afferents in cat primary visual cortex. Nat Neurosci 11:88-94. CrossRef Medline
25. Komban SJ, Alonso JM, Zaidi Q (2011) Darks are processed faster than lights. J Neurosci 31:8654-8658. CrossRef Medline
26. Kremers J, Lee BB, Pokorny J, Smith VC (1993) Responses of macaque ganglion cells and human observers to compound periodic waveforms. Vision Res 33:1997-2011. CrossRef Medline
27. Kuffler SW (1953) Discharge patterns and functional organization in the mammalian retina. J Neurophysiol 16:37-68. Medline
28. Manookin MB, Beaudoin DL, Ernst ZR, Flagel LJ, Demb JB (2008) Disinhibition combines with excitation to extend the operating range of the OFF visual pathway in daylight. J Neurosci 28:4136-4150. CrossRef Medline
29. Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4:877-886. CrossRef Medline
30. Meytlis M, Nichols Z, Nirenberg S (2012) Determining the role of correlated firing in large populations of neurons using white noise and natural scene stimuli. Vision Res 70:44-53. CrossRef Medline
31. Molnar A, Hsuch HA, Roska B, Werblin FS (2009) Crossover inhibition in the retina: circuitry that compensates for nonlinear rectifying synaptic transmission. J Comput Neurosci 27:569-590. CrossRef Medline
32. Moore DS, McCabe GP (2006) Introduction to the practice of statistics, Chapter 14. New York: W. H. Freeman.
33. Nikonov SS, Kholodenko R, Lem J, Pugh EN Jr (2006) Physiological features of the S- and M-cone photoreceptors of wild-type mice from single cell recordings. J Gen Physiol 127:359-374. CrossRef Medline
34. Nirenberg S, Pandarinath C (2012) Retinal prosthetic strategy with the capacity to restore normal vision. Proc Natl Acad Sci U S A 109:15012-15017. CrossRef Medline
35. Nirenberg S, Bomash I, Pillow JW, Victor JD (2010) Heterogeneous response dynamics in retinal ganglion cells: the interplay of predictive coding and adaptation. J Neurophysiol 103:3184-3194. CrossRef Medline
36. Oizumi M, Ishii T, Ishibashi K, Hosoya T, Okada M (2010) Mismatched decoding in the brain. J Neurosci 30:4815-4826. CrossRef Medline
37. Pandarinath C, Victor JD, Nirenberg S (2010) Symmetry breakdown in the ON and OFF pathways of the retina at night: functional implications. J Neurosci 30:10006-10014. CrossRef Medline
38. Paninski L, Pillow J, Lewi J (2007) Statistical models for neural encoding, decoding, and optimal stimulus design. Prog Brain Res 165:493-507. CrossRef Medline
39. Pillow JW, Shlens J, Paninski L, Sher A, Litke AM, Chichilnisky EJ, Simoncelli EP (2008) Spatio-temporal correlations and visual signalling in a complete neuronal population. Nature 454:995-999. CrossRef Medline
40. Pitkow X, Meister M (2012) Decorrelation and efficient coding by retinal ganglion cells. Nat Neurosci 15:628-635. CrossRef Medline
41. Press WH, Teukolsky SA, Vetterling WT, Flannery BP (2007) Random numbers. In: Numerical recipes, Ed 3, pp 397-401. Cambridge: MIT Press.
42. Rentería RC, Tian N, Cang J, Nakanishi S, Stryker MP, Copenhagen DR (2006) IntrinsicONresponses of the retinal OFF pathway are suppressed by the ON pathway. J Neurosci 26:11857-11869. CrossRef Medline
43. Sagdullaev BT, McCall MA (2005) Stimulus size and intensity alter fundamental receptive-field properties of mouse retinal ganglion cells in vivo. Vis Neurosci 22:649-659. Medline
44. Schiller PH (2010) Parallel information processing channels created in the retina. Proc Natl Acad Sci U S A 107:17087-17094. CrossRef Medline
45. Schwartz EA (1974) Responses of bipolar cells in the retina of the turtle. J Physiol 236:211-224. Medline
46. Simoncelli E, Paninski L, Pillow J, Schwartz O (2004) Characterization of neural responses with stochastic stimuli. In: Cognitive Neurosciences (Gazzaniga MS, ed), pp 327-328. Cambridge, MA: MIT.
47. Stone C, Pinto LH (1993) Response properties of ganglion cells in the isolated mouse retina. Vis Neurosci 10:31-39. CrossRef Medline
48. Umino Y, Solessio E, Barlow RB (2008) Speed, spatial, and temporal tuning of rod and cone vision in the mouse. J Neurosci 28:189-198. CrossRef Medline
49. Wang YV, Weick M, Demb JB (2011) Spectral and temporal sensitivity of cone-mediated responses in mouse retinal ganglion cells. J Neurosci 31: 7670-7681. CrossRef Medline
50. Wassle H (2004) Parallel processing in the mammalian retina. Nature Rev Neurosci 5:747-757. CrossRef
51. Werblin F, Dowling J (1969) Organization of the retina of the mudpuppy, Necurus maculosus. II. Intracellular recording. J Neurophysiol 32:39-355.
52. Xing D, Yeh CI, Shapley RM (2010) Generalization of black-dominant responses in V1 cortex. J Neurosci 30:13504-13512. CrossRef Medline
53. Yeh C, Xing D, Shapley R (2009) "Black" responses dominate macaque primary visual cortex V1. J Neurosci 23:11753-11760. Medline
54. Zaghloul KA, Boahen K, Demb JB (2003) Different circuits forONand OFF retinal ganglion cells cause different contrast sensitivities. J Neurosci 23: 2645-2654. Medline
55. Zemon V, Gordon J, Welch J (1988) Asymmetries in ON and OFF visual pathways of humans revealed using contrast-evoked cortical potentials. Visual Neurosci 1:145-150. CrossRef