Cortical-like receptive fields in the lateral geniculate nucleus of marmoset monkeys

Journal of Neuroscience

Volumn 33, Issue 16, 2013, Pages 6874-6876

  Cheong, Soon Keen ^a,b   Tailby, Chris ^a,c   Solomon, Samuel G ^a,d   Martin, Paul R ^a,b  

^a UNIVERSITY OF SYDNEY   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c FLOREY INSTITUTE OF NEUROSCIENCE AND MENTAL HEALTH   (Australia)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL TISSUE; ARTICLE; BINOCULAR VISION; CALLITHRIX; CLUSTER ANALYSIS; ELECTROCARDIOGRAPHY; ELECTRODE; ELECTROENCEPHALOGRAPHY; FEMALE; LATERAL GENICULATE BODY; MALE; NONHUMAN; ORIENTATION; PHOTORECEPTOR; PRIORITY JOURNAL; RECEPTIVE FIELD; SPATIAL FREQUENCY DISCRIMINATION; STRIATE CORTEX; VISUAL STIMULATION; ANIMAL; BIOLOGICAL MODEL; BRAIN MAPPING; EVOKED VISUAL RESPONSE; FOURIER ANALYSIS; GENICULATE BODY; HISTOLOGY; PHOTOSTIMULATION; PHYSIOLOGY; STATISTICAL MODEL; VISUAL CORTEX; VISUAL FIELD; VISUAL SYSTEM;

ANIMALS; BRAIN MAPPING; CALLITHRIX; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, VISUAL; FEMALE; FOURIER ANALYSIS; GENICULATE BODIES; LINEAR MODELS; MALE; MODELS, NEUROLOGICAL; ORIENTATION; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL FIELDS; VISUAL PATHWAYS;

MLCS; MLOWN;

EID: 84876216758     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5208-12.2013     Document Type: Article

References (86)

1. Alitto HJ, Moore BD 4th, Rathbun DL, Usrey WM (2011) A comparison of visual responsesinthe lateral geniculate nucleus of alert and anaesthetized macaque monkeys. J Physiol 589:87-99.
2. Alonso JM, Usrey WM, Reid RC (1996) Precisely correlated firing in cells of the lateral geniculate nucleus. Nature 383:815-819.
3. Benevento LA, Yoshida K (1981) The afferent and efferent organization of the lateral geniculo-prestriate pathways in the macaque monkey. J Comp Neurol 203:455-474.
4. Berens P (2009) CircStat: a MATLAB toolbox for circular statistics. J Stat Software 31.
5. Bishop PO, Burke W, Davis R (1962) The interpretation of the extracellular response of lateral geniculate cells. J Physiol 162:451-472.
6. Buzás P, Blessing EM, Szmajda BA, Martin PR (2006) Specificity of M and L cone inputs to receptive fields in the parvocellular pathway: random wiring with functional bias. J Neurosci 26:11148-11161.
7. Casagrande VA (1994) A third parallel visual pathway to primate area V1. Trends Neurosci 17:305-310.
8. Chapman B, Zahs KR, Stryker MP (1991) Relation of cortical cell orientation selectivity to alignment of receptive fields of the geniculocortical afferents that arborize within a single orientation column in ferret visual cortex. J Neurosci 11:1347-1358.
9. Chichilnisky EJ (2001) A simple white noise analysis of neuronal light responses. Network 12:199-213.
10. Croner LJ, Kaplan E (1995) Receptive fields of P and M ganglion cells across the primate retina. Vision Res 35:7-24.
11. Crook JM, Lange-Malecki B, Lee BB, Valberg A (1988) Visual resolution of macaque retinal ganglion cells. J Physiol 396:205-224.
12. Cynader M, Berman N (1972) Receptive-field organization of monkey superior colliculus. J Neurophysiol 35:187-201.
13. Dacey DM, Peterson BB, Robinson FR, Gamlin PD (2003) Fireworks in the primate retina: in vitro photodynamics reveals diverse LGN-projecting ganglion cell types. Neuron 37:15-27.
14. Dakin SC, Mareschal I, Bex PJ (2005) Local and global limitations on direction integration assessed using equivalent noise analysis. Vision Res 45: 3027-3049.
15. 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.
16. Derrington AM, Lennie P (1984) Spatial and temporal contrast sensitivities of neurones in lateral geniculate nucleus of macaque. J Physiol 357:219-240.
17. De Valois RL, Yund EW, Hepler N (1982) The orientation and direction selectivity of cells in macaque visual cortex. Vision Res 22:531-544.
18. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517-552.
19. Fitzpatrick D, Itoh K, Diamond IT (1983) The laminar organization of the lateral geniculate body and the striate cortex in the squirrel monkey (Sai-miri sciureus). J Neurosci 3:673-702.
20. Forte JD, Hashemi-Nezhad M, Dobbie WJ, Dreher B, Martin PR (2005) Spatial coding and response redundancy in parallel visual pathways of the marmoset Callithrix jacchus. Vis Neurosci 22:479-491.
21. Harting JK, Casagrande VA, Weber JT (1978) The projection of the primate superior colliculus upon the dorsal lateral geniculate nucleus: autoradio-graphic demonstration ofinterlaminar distribution of tectogeniculate ax-ons. Brain Res 150:593-599.
22. Harting JK, Hashikawa T, Van Lieshout D (1986) Laminar distribution of tectal, parabigeminal and pretectal inputs to the primate dorsal lateral geniculate nucleus: connectional studies in Galago crassicaudatus. Brain Res 366:358-363.
23. Harting JK, Van Lieshout DP, Hashikawa T, Weber JT (1991) The parabig-eminogeniculate projection: connectional studies in eight mammals. J Comp Neurol 305:559-581.
24. Hashemi-Nezhad M, Blessing EM, Dreher B, Martin PR (2008) Segregation of short-wavelength-sensitive ("blue") cone signals among neuronsin the lateral geniculate nucleus and striate cortex of marmosets. Vision Res 48:2604-2614.
25. He SG, Levick WR, Vaney DI (1998) Distinguishing direction selectivity from orientation selectivity in the rabbit retina. Visual Neurosci 15:439-447.
26. Heggelund P, Moors J (1983) Orientation selectivity and the spatial distribution of enhancement and suppression in receptive fields of cat striate cortex cells. Exp Brain Res 52:235-247.
27. Henry GH, Bishop PO, Dreher B (1974) Orientation, axis and direction as stimulus parameters for striate cells. Vision Res 14:767-777.
28. Hicks TP, Lee BB, Vidyasagar TR (1983) The responses of cells in macaque lateral geniculate nucleus to sinusoidal gratings. J Physiol 337:183-200.
29. Hubel DH, Wiesel TN (1977) Ferrier lecture. Functional architecture ofma-caque monkey visual cortex. Proc R Soc Lond B Biol Sci 198:1-59.
30. Irvin GE, Norton TT, Sesma MA, Casagrande VA (1986) W-like response properties of interlaminar zone cells in the lateral geniculate nucleus of a primate (Galago crassicaudatus). Brain Res 362:254-270.
31. Irvin GE, Casagrande VA, Norton TT (1993) Center/surround relationships of magnocellular, parvocellular, and koniocellular relay cells in primate lateral geniculate nucleus. Vis Neurosci 10:363-373.
32. Jin J, Wang Y, Swadlow HA, Alonso JM (2011) Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex. Nat Neurosci 14:232-238.
33. Kaplan E, Shapley RM (1986) The primate retina contains two types of ganglion cells, with high and low contrast sensitivity. Proc Natl Acad Sci U S A 83:2755-2757.
34. Kim IJ, Zhang Y, Yamagata M, Meister M, Sanes JR (2008) Molecular identification of a retinal cell type that responds to upward motion. Nature 452:478-482.
35. Lachica EA, Casagrande VA (1992) Direct W-like geniculate projections to the cytochrome oxidase (CO) blobs in primate visual cortex: axon morphology. J Comp Neurol 319:141-158.
36. Lee BB, Creutzfeldt OD, Elepfandt A (1979) The responses of magno- and parvocellular cells of the monkey's lateral geniculate body to moving stimuli. Exp Brian Res 35:547-557.
37. Lee BB, Pokorny J, Smith VC, Martin PR, Valberg A (1990) Luminance and chromatic modulation sensitivity of macaque ganglion cells and human observers. J Opt Soc Am A 7:2223-2236.
38. Lennie P, Movshon JA (2005) Coding of color and form in the geniculostri-ate visual pathway. J Opt Soc Am A Opt Image Sci Vis 22:2013-2033.
39. Leventhal AG, Schall JD (1983) Structural basis of orientation sensitivity of Cat Retinal Ganglion cells. J Comp Neurol 220:465-475.
40. Levick WR (1967) Receptive fields and trigger features of ganglion cells in the visual streak of the rabbits retina. J Physiol 188:285-307.
41. Levick WR, Thibos LN (1982) Analysis of orientation bias in cat retina. J Physiol 329:243-261.
42. 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.
43. Mardia KV, Jupp PE (2000) Directional statistics. New York: Wiley.
44. Marrocco RT, McClurkin JW, Young RA (1981) Spatial properties of superior colliculus cells projecting to the inferior pulvinar and parabigeminal nucleus of the monkey. Brain Res 222:150-154.
45. Mishkin M, Ungerleider LG, Macko KA (1983) Object vision and spatial vision: two cortical pathways. Trends Neurosci 6:414-417.
46. Naka K-I, Rushton WA (1966) S-potentials from colour units in the retina of fish (Cyprinidae). J Physiol 185:536-555.
47. Norton TT, Casagrande VA (1982) Laminar organization of receptive-field properties in lateral geniculate nucleus of bush baby (Galago crassicauda-tus). J Neurophysiol 47:715-741.
48. Paik SB, Ringach DL (2012) Link between orientation and retinotopic maps in primary visual cortex. Proc Natl Acad Sci U S A 109:7091-7096.
49. Passaglia CL, Troy JB, Rüttiger L, Lee BB (2002) Orientation sensitivity of ganglion cells in primate retina. Vision Res 42:683-694.
50. Piscopo DM, El-Danaf RN, Huberman AD, Niell CM (2013) Diverse visual features encodedin mouse lateral geniculate nucleus. JNeurosci 33:4642-4656.
51. Rodieck RW, Watanabe M (1993) Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae ofthe lateral geniculate nucleus. J Comp Neurol 338:289-303.
52. Schiller PH, Koerner F (1971) Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. J Neurophysiol 34:920-936.
53. Schmielau F, Singer W (1977) The role of visual cortex for binocular interactions in the cat lateral geniculate nucleus. Brain Res 120:354-361.
54. Sclar G, Maunsell JH, Lennie P (1990) Coding of image contrast in central visual pathways of the macaque monkey. Vision Res 30:1-10.
55. Shou TD, Leventhal AG (1989) Organized arrangement of orientation-sensitive relay cells in the cat's dorsal lateral geniculate nucleus. J Neurosci 9:4287-4302.
56. Sillito AM, Cudeiro J, Murphy PC (1993) Orientation sensitive elements in the corticofugal influence on centre-surround interactions in the dorsal lateral geniculate nucleus. Exp Brain Res 93:6-16.
57. Simpson JI (1984) The accessory optic system. Annu Rev Neurosci 7:13-41.
58. Sincich LC, Park KF, Wohlgemuth MJ, Horton JC (2004) Bypassing V1: a direct geniculate input to area MT. Nat Neurosci 7:1123-1128.
59. Sincich LC, Adams DL, Economides JR, Horton JC (2007) Transmission of spike trains at the retinogeniculate synapse. J Neurosci 27:2683-2692.
60. 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.
61. Smith EL 3rd, Chino YM, Ridder WH 3rd, Kitagawa K, Langston A (1990) Orientation bias of neurons in the lateral geniculate nucleus of macaque monkeys. Vis Neurosci 5:525-545.
62. Solomon SG, White AJ, Martin PR (1999) Temporal contrast sensitivity in the lateral geniculate nucleus of a New World monkey, the marmoset Callithrix jacchus. J Physiol 517:907-917.
63. Solomon SG, White AJ, Martin PR (2002) Extraclassical receptive field properties of parvocellular, magnocellular and koniocellular cells in the primate lateral geniculate nucleus. J Neurosci 22:338-349.
64. Solomon SG, Lee BB, Sun H (2006) Suppressive surrounds and contrast gain in magnocellular-pathway retinal ganglion cells of macaque. J Neu-rosci 26:8715-8726.
65. Solomon SG, Tailby C, Cheong SK, Camp AJ (2010) Linear and non-linear contributions to the visual sensitivity of neurons in primate lateral genic-ulate nucleus. J Neurophysiol 104:1884-1898.
66. Soodak RE, Shapley RM, Kaplan E (1987) Linear mechanism of orientation tuning in the retina and lateral geniculate nucleus of the cat. J Neuro-physiol 58:267-275.
67. Sun H, Smithson HE, Zaidi Q, Lee BB (2006) Do magnocellular and parvo-cellular ganglion cells avoid short-wavelength cone input? Vis Neurosci 23:441-446.
68. Szmajda BA, Buzás P, Fitzgibbon T, Martin PR (2006) Geniculocortical relay of blue-off signals in the primate visual system. Proc Natl Acad Sci U S A 103:19512-19517.
69. Szmajda BA, Grünert U, Martin PR (2008) Retinal ganglion cell inputs to the koniocellular pathway. J Comp Neurol 510:251-268.
70. Tailby C, Solomon SG, Dhruv NT, Majaj NJ, Sokol SH, Lennie P (2007) A new code for contrast in the primate visual pathway. J Neurosci 27:3904-3909.
71. Tailby C, Solomon SG, Lennie P (2008a) Functional asymmetries in visual pathways carrying S-cone signals in macaque. J Neurosci 28:4078-4087.
72. Tailby C, Szmajda BA, Buzás P, Lee BB, Martin PR (2008b) Transmission of blue (S) cone signals through the primate lateral geniculate nucleus. J Physiol 586:5947-5967.
73. Tailby C, Dobbie WJ, Hashemi-Nezhad M, Forte JD, Martin PR (2010) Receptive field asymmetries produce color-dependent direction selectivity in primate lateral geniculate nucleus. J Vis 10(8):1-18.
74. Tailby C, Cheong SK, Pietersen AN, Solomon SG, Martin PR (2012) Colour and pattern selectivity of receptive fields in superior colliculus of marmoset monkeys. J Physiol 590:4061-4077.
75. Usrey WM, Reid RC (2000) Visual physiology of the lateral geniculate nucleus in two species of New World monkey: Saimiri sciureus and Aotus trivirgatus. J Physiol 523:755-769.
76. Vaney DI, Sivyer B, Taylor WR (2012) Direction selectivity in the retina: symmetry and asymmetry in structure and function. Nat Rev Neurosci 13:194-208.
77. Venkataramani S, TaylorWR (2010) Orientation selectivity inrabbit retinal ganglion cells is mediated by presynaptic inhibition. J Neurosci 30: 15664-15676.
78. Vidyasagar TR, Urbas JV (1982) Orientation sensitivity of cat LGN neurones with and without inputs from visual cortical areas 17 and 18. Exp Brain Res 46:157-169.
79. Vidyasagar TR, Pei X, Volgushev M (1996) Multiple mechanisms underlying the orientation selectivityof visual cortical neurones. Trends Neurosci 19:272-277.
80. Wang W, Jones HE, Andolina IM, Salt TE, Sillito AM (2006) Functional alignment of feedback effects from visual cortex to thalamus. Nat Neuro-sci 9:1330-1336.
81. Warner CE, Goldshmit Y, Bourne JA (2010) Retinal afferents synapse with relay cells targeting the middle temporal area in the pulvinar and lateral geniculate nuclei. Front Neuroanat 4:8/1-8/16.
82. White AJ, Goodchild AK, Wilder HD, Sefton AJ, Martin PR (1998) Segregation of receptive field properties in the lateral geniculate nucleus of a New-World monkey, the marmoset Callithrix jacchus. J Neurophysiol 80:2063-2076.
83. White AJ, Solomon SG, Martin PR (2001) Spatial properties of koniocellu-lar cells in the lateral geniculate nucleus of the marmoset Callithrix jac-chus. J Physiol 533:519-535.
84. Xu X, Ichida JM, Allison JD, Boyd JD, Bonds AB, Casagrande VA (2001) A comparison of koniocellular, magnocellular and parvocellular receptive field properties in the lateral geniculate nucleus of the owl monkey (Aotus trivirgatus). J Physiol 531:203-218.
85. Xu X, Ichida J, Shostak Y, Bonds AB, Casagrande VA (2002) Are primate lateral geniculate nucleus (LGN) cells really sensitive to orientation or direction? Vis Neurosci 19:97-108.
86. Yukie M, Iwai E (1981) Direct projection from the dorsal lateral geniculate nucleus to the prestriate cortex in macaque monkeys. J Comp Neurol 201:81-97.