Temporal precision in the visual pathway through the interplay of excitation and stimulus-driven suppression

Journal of Neuroscience

Volumn 31, Issue 31, 2011, Pages 11313-11327

  Butts, Daniel A ^a   Weng, Chong ^b   Jin, Jianzhong ^b   Alonso, Jose Manuel ^b   Paninski, Liam ^c  

^a Bldg 142   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

^c Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACCURACY; ADAPTATION; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; CAT; CONTRAST; CONTROLLED STUDY; FEMALE; MALE; NERVE CELL INHIBITION; NERVE CELL STIMULATION; NONHUMAN; PRIORITY JOURNAL; SPIKE WAVE; THALAMUS; VISUAL STIMULATION; VISUAL SYSTEM;

ACTION POTENTIALS; ADAPTATION, PHYSIOLOGICAL; ANIMALS; CATS; FEMALE; GENICULATE BODIES; LINEAR MODELS; MALE; MODELS, NEUROLOGICAL; NERVE NET; NEURONS; NONLINEAR DYNAMICS; PARALYSIS; PHOTIC STIMULATION; REPRODUCIBILITY OF RESULTS; TIME PERCEPTION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

EID: 79961228048     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0434-11.2011     Document Type: Article

References (71)

1. Ahrens MB, Paninski L, Sahani M (2008) Inferring input nonlinearities in neural encoding models. Network 19:35-67.
2. Alitto HJ, Usrey WM (2008) Origin and dynamics of extraclassical suppression in the lateral geniculate nucleus of the macaque monkey. Neuron 57:135-146.
3. Allen EA, Freeman RD (2006) Dynamic spatial processing originates in early visual pathways. J Neurosci 26:11763-11774.
4. Berry MJ 2nd, Meister M (1998) Refractoriness and neural precision. J Neurosci 18:2200-2211.
5. Berry MJ 2nd, Brivanlou IH, Jordan TA, Meister M (1999) Anticipation of moving stimuli by the retina. Nature 398:334-338.
6. Blitz DM, Regehr WG (2005) Timing and specificity of feed-forward inhibition within the LGN. Neuron 45:917-928.
7. Borst A, Theunissen FE (1999) Information theory and neural coding. Nat Neurosci 2:947-957.
8. Brenner N, Strong SP, Koberle R, Bialek W, de Ruyter van Steveninck RR. (2000) Synergy in a neural code. Neural Comput 12:1531-1552.
9. Brillinger D (1992) Nerve cell spike train data analysis: a progression of technique. J Am Stat Assoc 87:260-271.
10. Buracas GT, Zador AM, DeWeese MR, Albright TD (1998) Efficient discrimination of temporal patterns by motion-sensitive neurons in primate visual cortex. Neuron 20:959-969.
11. Butts DA, Casti ARR (2009) Nonlinear computation performed at the retinogeniculate synapse. Soc Neurosci Abstr 35:849.5. Butts DA, Weng C, Jin J, Yeh CI, Lesica NA, Alonso JM, Stanley GB (2007) Temporal precision in the neural code and the timescales of natural vision. Nature 449:92-95.
12. Butts DA, Desbordes G, Weng C, Jin J, Alonso JM, Stanley GB (2010) The episodic nature of spike trains in the early visual pathway. J Neurophysiol 104:3371-3387.
13. 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.
14. Carandini M, Demb JB, Mante V, Tolhurst DJ, Dan Y, Olshausen BA, Gallant JL, Rust NC (2005) Do we know what the early visual system does? J Neurosci 25:10577-10597.
15. Carandini M, Horton JC, Sincich LC (2007) Thalamic filtering of retinal spike trains by postsynaptic title type=journal>summation. J Vis 7:20.1-2.11. Cardin JA, Palmer LA, Contreras D (2007) Stimulus feature selectivity in excitatory and inhibitory neurons in primary visual cortex. J Neurosci 27:10333-10344.
16. Casti A, Hayot F, Xiao Y, Kaplan E (2008) A simple model of retina-LGN transmission. J Comput Neurosci 24:235-252.
17. Chander D, Chichilnisky EJ (2001) Adaptation to temporal contrast in primate and salamander retina. J Neurosci 21:9904-9916.
18. Chichilnisky EJ (2001) A simple white noise analysis of neuronal light responses. Network 12:199-213.
19. Dawis S, Shapley R, Kaplan E, Tranchina D (1984) The receptive field organization of X-cells in the cat: spatiotemporal coupling and asymmetry. Vision Res 24:549-564.
20. de Ruyter van Steveninck R, Bialek W (1988) Real-time performance of a movement-sensitive neuron in the blowfly visual system: coding and information transfer in short spike sequences. Proc R Soc Lond B Biol Sci 234:379-414.
21. Desbordes G, Jin J, Weng C, Lesica NA, Stanley GB, Alonso JM (2008) Timing precision in population coding of natural scenes in the early visual system. PLoS Biol 6:e324. Dubin MW, Cleland BG (1977) Organization of visual inputs to interneurons of lateral geniculate nucleus of the cat. J Neurophysiol 40:410-427.
22. Fairhall AL, Burlingame CA, Narasimhan R, Harris RA, Puchalla JL, Berry MJ 2nd (2006) Selectivity for multiple stimulus features in retinal ganglion cells. J Neurophysiol 96:2724-2738.
23. Gabernet L, Jadhav SP, Feldman DE, Carandini M, Scanziani M (2005) Somatosensory integration controlled by dynamic thalamocortical feedforward inhibition. Neuron 48:315-327.
24. Gaudry KS, Reinagel P (2007) Contrast adaptation in a nonadapting LGN model. J Neurophysiol 98:1287-1296.
25. Gerstner W (2001) A framework for spiking neuron models: the spike response model. In: The handbook of biological physics, Vol 4 (Moss F, Gielen S, eds), pp 469-516. Amsterdam: Elsevier Sciences.
26. Kayser C, Kording KP, Konig P (2004) Processing of complex stimuli and natural scenes in the visual cortex. Curr Opin Neurobiol 14:468-473.
27. Keat J, Reinagel P, Reid RC, Meister M (2001) Predicting every spike: a model for the responses of visual neurons. Neuron 30:803-817.
28. Korenberg MJ, Sakai HM, Naka K (1989) Dissection of the neuron network in the catfish inner retina. III. Interpretation of spike kernels. J Neurophysiol 61:1110-1120.
29. Kouh M, Sharpee TO (2009) Estimating linear-nonlinear models using Renyi divergences. Network 20:49-68.
30. Kumbhani RD, Nolt MJ, Palmer LA (2007) Precision, reliability, and information-theoretic analysis of visual thalamocortical neurons. J Neurophysiol 98:2647-2663.
31. Lau B, Stanley GB, Dan Y (2002) Computational subunits of visual cortical neurons revealed by artificial neural networks. Proc Natl Acad Sci U S A 99:8974-8979.
32. Lesica NA, Stanley GB (2006) Decoupling functional mechanisms of adaptive encoding. Network 17:43-60.
33. Liu RC, Tzonev S, Rebrik S, Miller KD (2001) Variability and information in a neural code of the cat lateral geniculate nucleus. J Neurophysiol 86:2789-2806.
34. 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.
35. Mante V, Bonin V, Carandini M (2008) Functional mechanisms shaping lateral geniculate responses to artificial and natural stimuli. Neuron 58:625-638.
36. McCullagh P, Nelder J (1989) Generalized linear models. London: Chapman and Hall. Meister M, Berry MJ 2nd (1999) The neural code of the retina. Neuron 22:435-450.
37. Murphy GJ, Rieke F (2006) Network variability limits stimulus-evoked spike timing precision in retinal ganglion cells. Neuron 52:511-524.
38. Okun M, Lampl I (2008) Instantaneous correlation of excitation and inhibition during ongoing and sensory-evoked activities. Nat Neurosci 11:535-537.
39. Paninski L (2003) Convergence properties of three spike-triggered analysis techniques. Network 14:437-464.
40. Paninski L (2004) Maximum likelihood estimation of cascade pointprocess neural encoding models. Network 15:243-262.
41. Paninski L, Pillow JW, Lewi J (2007) Statistical models for neural encoding, decoding, and optimal stimulus design. In: Computational neuroscience: theoretical insights into brain function, Vol 165 (Cisek P, Drew T, Kalaska J, eds), pp 493-507. Boston: Elsevier Science
42. Paninski L, Ahmadian Y, Ferreira DG, Koyama S, Rahnama Rad K, Vidne M, Vogelstein J, Wu W (2010) A new look at state-space models for neural data. J Comput Neurosci 29:107-126.
43. Passaglia CL, Troy JB (2004) Information transmission rates of cat retinal ganglion cells. J Neurophysiol 91:1217-1229.
44. Pillow JW, Simoncelli EP (2006) Dimensionality reduction in neural models: an information-theoretic generalization of spike-triggered average and covariance analysis. J Vis 6:414-428.
45. Pillow JW, Paninski L, Uzzell VJ, Simoncelli EP, Chichilnisky EJ (2005) Prediction and decoding of retinal ganglion cell responses with a probabilistic spiking model. J Neurosci 25:11003-11013.
46. 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.
47. Prenger R, Wu MC, David SV, Gallant JL (2004) Nonlinear V1 responses to natural scenes revealed by neural network analysis. Neural Netw 17:663-679.
48. Priebe NJ, Ferster D (2006) Mechanisms underlying cross-orientation suppression in cat visual cortex. Nat Neurosci 9:552-561.
49. Rahnama Rad KR, Paninski L (2010) Efficient, adaptive estimation of twodimensional firing rate surfaces via Gaussian process methods. Network 21:142-168.
50. Rathbun DL, Warland DK, Usrey WM (2010) Spike timing and information transmission at retinogeniculate synapses. J Neurosci 30:13558-13566.
51. Reinagel P, Reid RC (2000) Temporal coding of visual information in the thalamus. J Neurosci 20:5392-5400.
52. Schwartz O, Simoncelli EP (2001) Natural signal statistics and sensory gain control. Nat Neurosci 4:819-825.
53. Schwartz O, Pillow JW, Rust NC, Simoncelli EP (2006) Spike-triggered neural characterization. J Vis 6:484-507.
54. Shapley R (2009) Linear and nonlinear systems analysis of the visual system: why does it seem so linear? A review dedicated to the memory of Henk Spekreijse. Vision Res 49:907-921 Shapley RM, Victor JD (1978) The effect of contrast on the transfer properties of cat retinal ganglion cells. J Physiol 285:275-298.
55. Shapley RM, Victor JD (1981) How the contrast gain control modifies the frequency responses of cat retinal ganglion cells. J Physiol 318:161-179.
56. Sharpee T, Rust NC, BialekW (2004) Analyzing neural responses to natural signals: maximally informative dimensions. Neural Comput 16:223-250.
57. Simoncelli EP, Pillow J, Paninski L, Schwartz O (2004) Characterization of neural responses with stochastic stimuli. In: The cognitive neurosciences (Gazzaniga M, ed), pp 327-338. Cambridge, MA: MIT
58. Sincich LC, Horton JC, Sharpee TO (2009) Preserving information in neural transmission. J Neurosci 29:6207-6216.
59. Theunissen F, Miller JP (1995) Temporal encoding in nervous systems: a rigorous definition. J Comput Neurosci 2:149-162.
60. Theunissen FE, David SV, Singh NC, Hsu A, Vinje WE, Gallant JL (2001) Estimating spatio-temporal receptive fields of auditory and visual neurons from their responses to natural stimuli. Network 12:289-316.
61. Truccolo W, Eden UT, Fellows MR, Donoghue JP, Brown EN (2005) A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. J Neurophysiol 93:1074-1089.
62. Uzzell VJ, Chichilnisky EJ (2004) Precision of spike trains in primate retinal ganglion cells. J Neurophysiol 92:780-789.
63. Wang X, Wei Y, Vaingankar V, Wang Q, Koepsell K, Sommer FT, Hirsch JA (2007) Feedforward excitation and inhibition evoke dual modes of firing in the cat's visual thalamus during naturalistic viewing. Neuron 55:465-478.
64. Wang X, Hirsch JA, Sommer FT (2010) Recoding of sensory information across the retinothalamic synapse. J Neurosci 30:13567-13577.
65. Wang X, Vaingankar V, Sanchez CS, Sommer FT, Hirsch JA (2011) Thalamic interneurons and relay cells use complementary synaptic mechanisms for visual processing. Nat Neurosci 14:224-231.
66. Wehr M, Zador AM (2003) Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426:442-446.
67. Weng C, Yeh CI, Stoelzel CR, Alonso JM (2005) Receptive field size and response latency are correlated within the cat visual thalamus. J Neurophysiol 93:3537-3547.
68. Wilent WB, Contreras D (2005) Dynamics of excitation and inhibition underlying stimulus selectivity in rat somatosensory cortex. Nat Neurosci 8:1364-1370.
69. Wu GK, Arbuckle R, Liu BH, Tao HW, Zhang LI (2008) Lateral sharpening of cortical frequency tuning by approximately balanced inhibition. Neuron 58:132-143.
70. Wu MC, David SV, Gallant JL (2006) Complete functional characterization of sensory neurons by system identification. Annu Rev Neurosci 29:477-505.
71. Zaghloul KA, Boahen K, Demb JB (2005) Contrast adaptation in subthreshold and spiking responses of mammalian Y-type retinal ganglion cells. J Neurosci 25:860-868.