The timing of response onset and offset in macaque visual neurons

Journal of Neuroscience

Volumn 22, Issue 8, 2002, Pages 3189-3205

  Bair, Wyeth ^a,b   Cavanaugh, James R ^b   Smith, Matthew A ^b   Movshon, J Anthony ^a,b  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NEW YORK UNIVERSITY   (United States)

Author keywords

Area MT V5; Inhibition; Integration time; Lateral geniculate nucleus; Macaque monkey; Primary visual cortex; Response latency; Spike timing; Spontaneous activity; Temporal dynamics

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; GIANT CELL; LATENT PERIOD; LATERAL GENICULATE BODY; MACACA; NERVE CONDUCTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VISION; VISUAL CORTEX; VISUAL NERVOUS SYSTEM; VISUAL STIMULATION;

EID: 0037092434     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-08-03189.2002     Document Type: Article

References (115)

1. Adelson EH, Bergen JR (1985) Spatiotemporal energy models for the perception of motion. J Opt Soc Am A 2:284-299.
2. Adrian ED, Matthews R (1927) The action of light on the eye. Part I. The discharge of impulses in the optic never and its relation to the electric changes in the retina. J Physiol (Lond) 63:378-414.
3. Agmon A, Connors BW (1992) Correlation between intrinsic firing patterns and thalamocortical synaptic responses of neurons in mouse barrel cortex. J Neurosci 12:319-329.
4. Ahissar E, Sosnik R, Haidarliu S (2000) Transformation from temporal to rate coding in a somatosensory thalamocortical pathway. Nature 406:302-306.
5. Albright TD, Desimone R, Gross CG (1984) Columnar organization of directionally selective cells in visual area MT of the macaque. J Neurophysiol 51:16-31.
6. Azouz R, Gray CM (1999) Cellular mechanisms contributing to response variability of cortical neurons in vivo. J Neurosci 19:2209-2223.
7. Bair W, Koch C (1996) Temporal precision of spike trains in extrastriate cortex. Neural Comput 8:1185-1202.
8. Bair W, Cavanaugh JR, Movshon JA (1997) Reconstructing stimulus velocity from neuronal responses in area MT. In: Advances in Neural Information Processing Systems, Vol 9 (Mozer MC, Jordan MI, Petsche T, eds), pp 34-40. Cambridge, MA: MIT.
9. Bair W, Cavanaugh JR, Smith MA, Movshon JA (2001) Switching between off and on in the macaque visual system. Paper presented at the annual meeting of the Vision Sciences Society, Sarasota, FL, May.
10. Barlow HB (1953) Summation and inhibition in the frog's retina. J Physiol (Lond) 119:69-88.
11. Barlow HB, Hill RM (1963) Evidence for a physiological explanation of the waterfall phenomenon and figural after-effects. Nature 200:1345-1347.
12. Bartlett JR, Doty RW (1974) Response of units in striate cortex of squirrel monkeys to visual and electrical stimuli. J Neurophysiol 37:621-641.
13. Benardete EA, Kaplan E (1997) The receptive field of the primate P retinal ganglion cell, I: Linear dynamics. Vis Neurosci 14:169-185.
14. Benardete EA, Kaplan E (1999) The dynamics of primate M retinal ganglion cells. Vis Neurosci 16:355-368.
15. Benardete EA, Kaplan E, Knight BW (1992) Contrast gain control in the primate retina: P cells are not X-like, some M cells are. Vis Neurosci 8:483-486.
16. Borg-Graham LJ, Monier C, Fregnac Y (1998) Visual input evokes transient and strong shunting inhibition in visual cortical neurons. Nature 393:369-373.
17. Carandini M, Ferster D (1997) A tonic hyperpolarization underlying contrast adaptation in cat visual cortex. Science 276:949-952.
18. Carandini M, Ferster D (2000) Membrane potential and firing rate in cat primary visual cortex. J Neurosci 20:470-484.
19. Carandini M, Mechler R, Leonard CS, Movshon JA (1996) Spike train encoding by regular-spiking cells of the visual cortex. J Neurophysiol 76:3425-3441.
20. Carandini M, Heeger DJ, Movshon JA (1997) Linearity and normalization in simple cells of the macaque primary visual cortex. J Neurosci 17:8621-8644.
21. Casagrande VA, Norton TT (1991) Lateral geniculate nucleus: A review of its physiology and function. In: Vision and Visual Dysfunction: The Neural Basis of Visual Function, Vol 4, (Leventhal AG, ed), pp 41-84. London: Macmillan.
22. Celebrini S, Thorpe S, Trotter Y, Imbert M (1993) Dynamics of orientation coding in area V1 of the awake primate. Vis Neurosci 10:811-825.
23. Cleland BG, Dubin MW, Levick WR (1971) Sustained and transient neurones in the cat's retina and lateral geniculate nucleus. J Physiol (Lond) 217:473-496.
24. Coenen AML, Vendrik AJH (1972) Determination of the transfer ratio of cat's geniculate neurons through quasi-intracellular recordings and the relation with the level of alertness. Exp Brain Res 14:227-242.
25. Coenen AML, Gerrits HJM, Vendrik AJH (1972) Analysis of the response characteristics of optic tract and geniculate units and their mutual relationship. Exp Brain Res 15:452-471.
26. Creutzfeldt O, Ito M (1968) Functional synaptic organization of primary visual cortex neurones in the cat. Exp Brain Res 6:324-352.
27. Creutzfeldt O, Sakmann B (1969) Neurophysiology of vision. Annu Rev Physiol 31:499-544.
28. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol (Lond) 187:517-552.
29. Eysel UT, Shevelev IA, Lazareva NA, Sharaev GA (1998) Orientation tuning and receptive field structure in cat striate neurons during local blockade of intracortical inhibition. Neuroscience 84:25-36.
30. Ferster D (1988) Spatially opponent excitation and inhibition in simple cells of the cat visual cortex. J Neurosci 8:1172-1180.
31. Ferster D, Miller KD (2000) Neural mechanisms of orientation selectivity in the visual cortex. Annu Rev Neurosci 23:441-471.
32. Freund TF, Martin KAC, Somogyi P, Whitteridge D (1985) Innervation of cat visual areas 17 and 18 by physiologically identified X- and Y-type thalamic afferents. II. Identification of postsynaptic targets by GABA immunocytochemistry and Golgi impregnation. J Comp Neurol 242:275-291.
33. Gautrais J, Thorpe S (1998) Rate coding versus temporal order coding: A theoretical approach. Biosystems 48:57-65.
34. Gawne TJ, Kjaer TW, Richmond BJ (1996) Latency: Another potential code for feature binding in striate cortex. J Neurophysiol 76:1356-1360.
35. 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.
36. Heeger DJ, Boynton GM, Demb JB, Seidemann E, Newsome WT (1999) Motion opponency in visual cortex. J Neurosci 19:7162-7174.
37. Heggelund P (1986) Quantitative studies of enhancement and suppression zones in the receptive field of simple cells in cat striate cortex. J Physiol (Lond) 373:293-310.
38. Herz A, Creutzfeldt O, Fuster J (1964) Statistische Eigenschaften der Neuronaktivität im ascendierenden visuellen System. Kybernetik 2:61-71.
39. Hirsch JA, Alonso J-M, Reid RC, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18:9517-9528.
40. Hopfield JJ (1995) Pattern recognition computation using action potential timing for stimulus representation. Nature 376:33-36.
41. Hubel DH, Wiesel TN (1959) Receptive fields of single neurons in the cat's striate cortex. J Physiol (Lond) 148:574-591.
42. Hubel DH, Wiesel TN (1961) Integrative action in the cat's lateral geniculate body. J Physiol (Lond) 155:385-398.
43. Humphrey AL, Weller RE (1988) Functionally distinct groups of X-cells in the lateral geniculate nucleus of the cat. J Comp Neurol 268:429-447.
44. Jones R, Keck MJ (1978) Visual evoked response as a function of grating spatial frequency. Invest Ophthalmol Vis Sci 17:652-659.
45. Kaplan E, Mukherjee P, Shapley R (1993) Information filtering in the lateral geniculate nucleus. In: Contrast Sensitivity, Vol 5 (Shapley R, Lam M-K, eds), pp 183-200. Cambridge, MA: MIT.
46. Kawano K, Shidara M, Watanabe Y, Yamane S (1994) Neural activity in cortical area MST of alert monkey during ocular following responses. J Neurophysiol 71:2305-2324.
47. Kiang NY-S, Watanabe T, Thomas EC, Clark LF (1965) Discharge Patterns of Single Fibers in the Cat's Auditory Nerve. Cambridge, MA: MIT.
48. Kiang NY-S, Lieberman MC, Levire RA (1976) Auditory-nerve activity in cats exposed to ototoxic drugs and high-intensity sounds. Ann Otol Rhinol Laryngol 85:752-768.
49. Kuffler SW (1953) Discharge patterns and functional organization of mammalian retina. J Neurophysiol 16:37-68.
50. Lagae L, Raiguel S, Orban GA (1993) Speed and direction selectivity of macaque middle temporal neurons. J Neurophysiol 69:19-39.
51. Lapicque L (1907) Recherches quantitatives sur l'excitation electrique des nerfs traitée comme une polarisation. J Physiol (Lond) 9:620-635.
52. Lee BB (1996) Receptive field structure in the primate retina. Vision Res 36:631-644.
53. Lee BB, Pokorny J, Smith VC, Kremers J (1994) Responses to pulses and sinusoids in macaque ganglion cells. Vision Res 34:3081-3096.
54. Lennie P (2000) Color vision: Putting it together. Curr Biol 10:R589-R591.
55. Lennie P, Haake W, Williams DR (1991) The design of chromatically opponent receptive fields. In: Computational Models of Visual Processing (Landy MS, Movshon JA, eds), pp 71-82. Cambridge, MA: MIT.
56. Levick WR (1973) Variation in the response latency of cat retinal ganglion cells. Vision Res 13:837-853.
57. Levitt JB, Schumer RA, Sherman SM, Spear PD, Movshon JA (2001) Visual response properties of neurons in the LGN of normally-reared and visually-deprived macaque monkeys. J Neurophysiol 85:2111-2129.
58. Lisberger SG, Movshon JA (1999) Visual motion analysis for pursuit eye movements in area MT of macaque monkeys. J Neurosci 19:2224-2246.
59. Marvślek P, Koch C, Maunsell J (1997) On the relationship between synaptic input and spike output jitter in individual neurons. Proc Natl Acad Sci USA 94:735-740.
60. Mastronarde DN (1987a) Two classes of single-input X-cells in cat lateral geniculate nucleus. I. Receptive field properties and classification of cells. J Neurophysiol 57:357-380.
61. Mastronarde DN (1987b) Two classes of single-input X-cells in cat lateral geniculate nucleus. II. Retinal inputs and the generation of receptive-field properties. J Neurophysiol 57:381-413.
62. Maunsell JHR, Gibson JR (1992) Visual response latencies in striate cortex of the macaque monkey. J Neurophysiol 68:1332-1344.
63. Maunsell JHR, Van Essen DC (1983) Functional properties of neurons in middle temporal visual area of the macaque monkey. I. Selectivity for stimulus direction, speed, and orientation. J Neurophysiol 49:1127-1147.
64. Maunsell JHR, Ghose GM, Assad JA, McAdams CJ, Boudreau CE, Noerager BD (1999) Visual response latencies of magnocellular and parvocellular LGN neurons in macaque monkeys. Vis Neurosci 16:1-14.
65. McIlwain JT, Creutzfeldt OD (1967) Microelectrode study of synaptic excitation and inhibition in the lateral geniculate nucleus of the cat. J Neurophysiol 30:1-21.
66. Merrill EG, Ainsworth A (1972) Glass-coated platinum-plated tungsten microelectrode. Med Biol Eng 10:662-672.
67. Middlebrooks JC, Clock AE, Xu L, Green DM (1994) A panoramic code for sound location by cortical neurons. Science 264:842-844.
68. Mitzdorf U, Singer W (1979) Excitatory synaptic ensemble properties in the visual cortex of the macaque monkey: A current source density analysis of electrically evoked potentials. J Comp Neurol 187:71-84.
69. Movshon JA, Newsome WT (1996) Visual response properties of striate cortical neurons projecting to area MT in macaque monkeys. J Neurosci 16:7733-7741.
70. Movshon JA, Thompson ID, Tolhurst DJ (1978) Spatial summation in the receptive fields of simple cells in the cat's striate cortex. J Physiol (Lond) 283:53-77.
71. Movshon JA, Adelson EH, Gizzi MS, Newsome WT (1985) The analysis of moving visual patterns. In: Study Group on Pattern Recognition Mechanisms (Chagas C, Gattass R, Gross CG, eds), pp 118-151. Vatican City: Pontificia Academia Scientiarum.
72. Movshon JA, Lisberger SG, Krauzlis RJ (1990) Visual cortical signals supporting smooth pursuit eye movements. In: Cold Spring Harbor Symposia on Quantitative Biology, Vol LV, pp 707-716. New York: CSH.
73. Nowak LG, Bullier J (1997) The timing of information transfer in the visual system. In: Cerebral Cortex, Extrastriate Cortex in Primates, Vol 12 (Rocklund K, Kaas J, Peters A, eds), pp 205-241. New York: Plenum.
74. Nowak LG, Munk MHJ, Girard P, Bullier J (1995) Visual latencies in areas V1 and V2 of the macaque monkey. Vis Neurosci 12:371-384.
75. Nowak LG, Sanchez-Vives MV, McCormick DA (1997) Influence of low and high frequency inputs on spike timing in visual cortical neurons. Cereb Cortex 7:487-501.
76. O'Keefe LP, Movshon JA (1998) Processing of first- and second-order motion signals by neurons in area MT of the macaque monkey. Vis Neurosci 15:305-317.
77. Palmer LA, Davis TL (1981) Receptive-field structure in cat striate cortex. J Neurophysiol 46:260-276.
78. Parker DM, Salzen EA (1977) Latency changes in the human visual evoked response to sinusoidal gratings. Vision Res 17:1201-1204.
79. Pettigrew JD, Nikara T, Bishop PO (1968) Responses to moving slits by single units in cat striate cortex. Exp Brain Res 6:373-390.
80. Porter JT, Johnson CK, Agmon A (2001) Diverse types of interneurons generate thalamus-evoked feedforward inhibition in the mouse barrel cortex. J Neurosci 21:2699-2710.
81. Press HP, Teukolsky SA, Vetterling WT, Flannery BP (1992) Numerical Recipes in C, the Art of Scientific Computing, Ed 2. Cambridge: Cambridge UP.
82. Qian N, Andersen RA (1994) Transparent motion perception as detection of unbalanced motion signals, 2. Physiology. J Neurosci 14:7367-7380.
83. Raiguel SE, Lagae L, Gulyás B, Orban GA (1989) Response latencies of visual cells in macaque areas V1, V2 and V5. Brain Res 493:155-159.
84. Raiguel SE, Xiao D-K, Marcar VL, Orban GA (1999) Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters. J Neurophysiol 82:1944-1956.
85. Raymond J, Braddick O (1996) Responses to opposed directions of motion: Continuum or independent mechanisms? Vision Res 36:1931-1937.
86. Reid RC, Alonso JM (1995) Specificity of monosynaptic connections from thalamus to visual cortex. Nature 378:281-284.
87. Reid RC, Victor JD, Shapley RM (1992) Broadband temporal stimuli decrease the integration time of neurons in cat striate cortex. Vis Neurosci 9:39-45.
88. Reid RC, Victor JD, Shapley RM (1997) The use of m-sequences in the analysis of visual neurons: Linear receptive field properties. Vis Neurosci 14:1015-1027.
89. Rockland KS (1995) Morphology of individual axons projecting from area V2 to MT in the macaque. J Comp Neurol 355:15-26.
90. Sanchez-Vives MV, Nowak LG, McCormick DA (2000) Membrane mechanisms underlying contrast adaptation in cat area 17 in vivo. J Neurosci 20:4267-4285.
91. Saul AB (1995) Adaptation aftereffects in single neurons of cat visual cortex: Response timing is retarded by adapting. Vis Neurosci 12:191-205.
92. Saul AB, Humphrey AL (1990) Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus. J Neurophysiol 64:206-224.
93. Schiller PH (1992) The ON and OFF channels of the visual system. Trends Neurosci 15:86-92.
94. Schmolesky MT, Wang Y, Hanes DP, Thompson KG, Leutgeb S, Schall JD, Leventhal AG (1998) Signal timing across the macaque visual system. J Neurophysiol 79:3272-3278.
95. Sestokas AK, Lehmkuhle S (1986) Visual response latency of X- and Y-cells in the dorsal lateral geniculate nucleus of the cat. Vision Res 26:1041-1054.
96. Shapley RM, Victor JD (1978) The effect of contrast on the transfer properties of cat retinal ganglion cells. J Physiol (Lond) 285:275-298.
97. Sherman SM, Koch C (1986) The control of retinogeniculate transmission in the mammalian lateral geniculate nucleus. Exp Brain Res 63:1-20.
98. Sillito AM (1975) The contribution of inhibitory mechanisms to the receptive field properties of neurons in the striate cortex of the cat. J Physiol (Lond) 250:305-329.
99. Singer W, Creutzfeldt OD (1970) Reciprocal lateral inhibition of on- and off-center neurones in the lateral geniculate body of the cat. Exp Brain Res 10:311-330.
100. Singer W, Pöppel E, Creutzfeldt OD (1970) Inhibitory interactions in the cat's lateral geniculate nucleus. Exp Brain Res 14:210-226.
101. Skottun BC, De Valois RL, Grosof DH, Movshon JA, Albrecht DG, Bonds AB (1991) Classifying simple and complex cells on the basis of response modulation. Vision Res 31:1079-1086.
102. Snodderly DM, Gur M (1995) Organization of striate cortex of alert, trained monkeys (Macaca fascicularis): Ongoing activity, stimulus selectivity, and widths of receptive field activating regions. J Neurophysiol 74:2100-2125.
103. Sutherland NS (1961) Figural aftereffects and apparent size. Q J Exp Psychol 13:222-228.
104. Sutter EE (1987) A practical non-stochastic approach to nonlinear time-domain analysis. In: Advanced methods of physiological systems modeling, Vol 1 (Marmaerelis V, ed), pp 303-315. Los Angeles, CA: University of Southern California.
105. Swadlow HA (1995) Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: Evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation. J Neurophysiol 73:1584-1599.
106. Tamás G, Buhl EH, Somogyi P (1997) Fast IPSPs elicited via multiple synaptic release sites by different types of GABAergic neurons in the cat visual cortex. J Physiol (Lond) 500:715-738.
107. Tolhurst DJ, Dean AF (1990) The effects of contrast on the linearity of spatial summation of simple cells in the cat's striate cortex. Exp Brain Res 79:582-588.
108. Troyer TW, Krukowski AE, Priebe NJ, Miller KD (1998) Contrast-invariant orientation tuning in cat visual cortex: Thalomocortical input tuning and correlation-based intracortical connectivity. J Neurosci 18:5908-5927.
109. Usrey WM, Reppas JB, Reid RC (1998) Paired-spike interactions and synaptic efficacy of retinal inputs to the thalamus. Nature 395:384-387.
110. Vautin RG, Berkley MA (1977) Responses of single cells in cat visual cortex to prolonged stimulus movement: Neural correlates of visual aftereffects. J Neurophysiol 40:1051-1065.
111. Volgushev M, Vidyasagar TR, Pei X (1995) Dynamics of the orientation tuning of postsynaptic potentials in the cat visual cortex. Vis Neurosci 12:621-628.
112. von Baumgarten R, Jung R (1952) Microelectrode studies on the visual cortex. Rev Neurol (Paris) 87:151-155.
113. Wang C, Cleland BG, Burke W (1985) Synaptic delay in the lateral geniculate nucleus of the cat. Brain Res 343:236-245.
114. Wielaard DJ, Shelley M, McLaughlin D, Shapley R (2001) How simple cells are made in a nonlinear network model of the visual cortex. J Neurosci 21:5203-5211.
115. Zeki SM (1974) Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J Physiol (Lond) 236:549-573.