Luminance-evoked inhibition in primary visual cortex: A transient veto of simultaneous and ongoing response

Journal of Neuroscience

Volumn 26, Issue 52, 2006, Pages 13537-13547

  Tucker, Thomas R ^a,b   Fitzpatrick, David ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b GUILFORD COLLEGE   (United States)

Author keywords

Inhibition; Luminance; Neural circuits; Physiology; Synaptic conductance; Visual cortex

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; EXCITATION; INHIBITORY POSTSYNAPTIC POTENTIAL; LUMINANCE; NERVE; NERVE POTENTIAL; NONHUMAN; ORIENTATION; PRIORITY JOURNAL; SHREW; VISION; VISUAL CORTEX; VISUAL STIMULATION;

ACTION POTENTIALS; ANIMALS; EVOKED POTENTIALS, VISUAL; NEURAL INHIBITION; NEURONS; PHOTIC STIMULATION; PHOTOTRANSDUCTION; REACTION TIME; TUPAIIDAE; VISUAL CORTEX;

EID: 33845877970     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3723-06.2006     Document Type: Article

References (62)

1. Alitto HJ, Weyand TG, Usrey WM (2005) Distinct properties of stimulus-evoked bursts in the lateral geniculate nucleus. J Neurosci 25:514-523.
2. Anderson JS, Carandini M, Ferster D (2000) Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J Neurophysiol 84:909-926.
3. Beierlein M, Gibson JR, Connors BW (2003) Two dynamically distinct inhibitory networks in layer 4 of the neocortex. J Neurophysiol 90:2987-3000.
4. Bosking WH, Zhang Y, Schofield B, Fitzpatrick D (1997) Orientation selectivity and the arrangement of horizontal connections in tree shrew striate cortex. J Neurosci 17:2112-2127.
5. Boynton RM, Kandel G (1957) On responses in the human visual system as a function of adaptation level. J Opt Soc Am 47:275-286.
6. Brainard DH (1997) The psychophysics toolbox. Spat Vis 10:433-436.
7. Breitmeyer BG, Ogmen H (2000) Recent models and findings in visual backward masking: a comparison, review, and update. Percept Psychophys 62:1572-1595.
8. Bridgeman B (1971) Metacontrast and lateral inhibition. Psychol Rev 78:528-539.
9. Bridgeman B (1975) Correlates of metacontrast in single cells of the cat visual system. Vision Res 15:91-99.
10. Bruno RM, Simons DJ (2002) Feedforward mechanisms of excitatory and inhibitory cortical receptive fields. J Neurosci 22:10966-10975.
11. Callaway EM (1998) Local circuits in primary visual cortex of the macaque monkey. Annu Rev Neurosci 21:47-74.
12. Chisum HJ, Mooser F, Fitzpatrick D (2003) Emergent properties of layer 2/3 neurons reflect the collinear arrangement of horizontal connections in tree shrew visual cortex. J Neurosci 23:2947-2960.
13. Crawford BH (1947) Visual adaptation in relation to brief conditioning stimuli. Proc R Soc Lond B Biol Sci 134:283-302.
14. Denning KS, Reinagel P (2005) Visual control of burst priming in the anesthetized lateral geniculate nucleus. J Neurosci 25:3531-3538.
15. Douglas RJ, Martin KA (2004) Neuronal circuits of the neocortex. Annu Rev Neurosci 27:419-451.
16. Ferster D (1986) Orientation selectivity of synaptic potentials in neurons of cat primary visual cortex. J Neurosci 6:1284-1301.
17. Ferster D, Jagadeesh B (1992) EPSP-IPSP interactions in cat visual cortex studied with in vivo whole-cell patch recording. J Neurosci 12:1262-1274.
18. Ferster D, Chung S, Wheat H (1996) Orientation selectivity of thalamic input to simple cells of cat visual cortex. Nature 380:249-252.
19. Fitzpatrick D (1996) The functional organization of local circuits in visual cortex: insights from the study of tree shrew striate cortex. Cereb Cortex 6:329-341.
20. Gawne TJ, Martin JM (2000) Activity of primate V1 cortical neurons during blinks. J Neurophysiol 84:2691-2694.
21. Gawne TJ, Martin JM (2002) Responses of primate visual cortical neurons to stimuli presented by flash, saccade, blink, and external darkening. J Neurophysiol 88:2178-2186.
22. Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75-79.
23. Haynes JD, Lotto RB, Rees G (2004) Responses of human visual cortex to uniform surfaces. Proc Natl Acad Sci USA 101:4286-4291.
24. Hirsch JA, Alonso JM, Reid RC, Martinez LM (1998) Synaptic integration in striate cortical simple cells. J Neurosci 18:9517-9528.
25. Hirsch JA, Martinez LM, Pillai C, Alonso JM, Wang Q, Sommer FT (2003) Functionally distinct inhibitory neurons at the first stage of visual cortical processing. Nat Neurosci 6:1300-1308.
26. Huang X, Paradiso MA (2005) Background changes delay information represented in macaque V1 neurons. J Neurophysiol 94:4314-4330.
27. Huang X, Blau S, Paradiso MA (2005) Background changes delay the perceptual availability of form information. J Neurophysiol 94:4331-4343.
28. Hubel DH (1960) Single unit activity in lateral geniculate body and optic tract of unrestrained cats. J Physiol (Lond) 150:91-104.
29. Hubel DH, Wiesel TN (1961) Integrative action in the cat's lateral geniculate body. J Physiol (Lond) 155:385-398.
30. Jacobs GH, Yolton RL (1970) Center-surround balance in receptive fields of cells in the lateral geniculate nucleus. Vision Res 10:1127-1144.
31. Kammer T, Lehr L, Kirschfeld K (1999) Cortical visual processing is temporally dispersed by luminance in human subjects. Neurosci Lett 263:133-136.
32. Kara P, Pezaris JS, Yurgenson S, Reid RC (2002) The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation. Proc Natl Acad Sci USA 99:16261-16266.
33. Kayama Y, Riso RR, Bartlett JR, Doty RW (1979) Luxotonic responses of units in macaque striate cortex. J Neurophysiol 42:1495-1517.
34. Kinoshita M, Komatsu H (2001) Neural representation of the luminance and brightness of a uniform surface in the macaque primary visual cortex. J Neurophysiol 86:2559-2570.
35. Kolers P, Rosner BS (1960) On visual masking (metacontrast): dichoptic observations. Am J Psychol 73:2-21.
36. Komatsu H, Murakami I, Kinoshita M (1996) Surface representation in the visual system. Brain Res Cogn Brain Res 5:97-104.
37. Kretz R, Rager G, Norton TT (1986) Laminar organization of ON and OFF regions and ocular dominance in the striate cortex of the tree shrew (Tupaia belangeri). J Comp Neurol 251:135-145.
38. Leopold DA, Logothetis NK (1996) Activity changes in early visual cortex reflect monkeys' percepts during binocular rivalry. Nature 379:549-553.
39. Lesica NA, Stanley GB (2004) Encoding of natural scene movies by tonic and burst spikes in the lateral geniculate nucleus. J Neurosci 24:10731-10740.
40. Lund JS (1988) Anatomical organization of macaque monkey striate visual cortex. Annu Rev Neurosci 11:253-288.
41. Lund JS, Angelucci A, Bressloff PC (2003) Anatomical substrates for functional columns in macaque monkey primary visual cortex. Cereb Cortex 13:15-24.
42. Macknik SL, Livingstone MS (1998) Neuronal correlates of visibility and invisibility in the primate visual system. Nat Neurosci 1:144-149.
43. Macknik SL, Martinez-Conde S (2004) Dichoptic visual masking reveals that early binocular neurons exhibit weak interocular suppression: implications for binocular vision and visual awareness. J Cogn Neurosci 16:1049-1059.
44. Macknik SL, Martinez-Conde S, Haglund MM (2000) The role of spatiotemporal edges in visibility and visual masking. Proc Natl Acad Sci USA 97:7556-7560.
45. Marrocco RT (1972) Maintained activity of monkey optic tract fibers and lateral geniculate nucleus cells. Vision Res 12:1175-1181.
46. Martinez-Conde S, Macknik SL, Hubel DH (2002) The function of bursts of spikes during visual fixation in the awake primate lateral geniculate nucleus and primary visual cortex. Proc Natl Acad Sci USA 99:13920-13925.
47. Monier C, Chavane F, Baudot P, Graham LJ, Fregnac Y (2003) Orientation and direction selectivity of synaptic inputs in visual cortical neurons: a diversity of combinations produces spike tuning. Neuron 37:663-680.
48. Mooser F, Bosking WH, Fitzpatrick D (2004) A morphological basis for orientation tuning in primary visual cortex. Nat Neurosci 7:872-879.
49. Mukhametov LM, Rizzolatti G (1970) The responses of lateral geniculate neurons to flashes of light during the sleep-waking cycle. Arch Ital Biol 108:348-368.
50. Muly EC, Fitzpatrick D (1992) The morphological basis for binocular and ON/OFF convergence in tree shrew striate cortex. J Neurosci 12:1319-1334.
51. Ogmen H, Breitmeyer BG, Melvin R (2003) The what and where in visual masking. Vision Res 43:1337-1350.
52. Pelli DG (1997) The VideoToolbox software for visual psychophysics: transforming numbers into movies. Spat Vis 10:437-442.
53. Peng X, Van Essen DC (2005) Peaked encoding of relative luminance in macaque areas V1 and V2. J Neurophysiol 93:1620-1632.
54. 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.
55. Ramcharan EJ, Gnadt JW, Sherman SM (2001) The effects of saccadic eye movements on the activity of geniculate relay neurons in the monkey. Vis Neurosci 18:253-258.
56. Schiller PH (1965) Monoptic and dichoptic visual masking by patterns and flashes. J Exp Psychol 69:193-199.
57. Schiller PH (1968) Single unit analysis of backward visual masking and metacontrast in the cat lateral geniculate nucleus. Vision Res 8:855-866.
58. Sherman SM (2001) Tonic and burst firing: dual modes of thalamocortical relay. Trends Neurosci 24:122-126.
59. Swadlow HA (2003) Fast-spike interneurons and feedforward inhibition in awake sensory neocortex. Cereb Cortex 13:25-32.
60. Swadlow HA, Gusev AG (2001) The impact of "bursting" thalamic impulses at a neocortical synapse. Nat Neurosci 4:402-408.
61. Valberg A, Lee BB, Tigwell DA, Creutzfeldt OD (1985) A simultaneous contrast effect of steady remote surrounds on responses of cells in macaque lateral geniculate nucleus. Exp Brain Res 58:604-608.
62. Wilke M, Logothetis NK, Leopold DA (2003) Generalized flash suppression of salient visual targets. Neuron 39:1043-1052.