Neuronal responses to face-like and facial stimuli in the monkey superior colliculus

Frontiers in Behavioral Neuroscience

Volumn 8, Issue MAR, 2014, Pages

  Nguyen, Minh Nui ^a   Matsumoto, Jumpei ^a   Hori, Etsuro ^a   Maior, Rafael Souto ^b   Tomaz, Carlos ^b   Tran, Anh H ^a   Ono, Taketoshi ^a   Nishijo, Hisao ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

^b UNIVERSITY OF BRASILIA   (Brazil)

Author keywords

Face; Face like patterns; Monkey; Subcortical pathway; Superior colliculus

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; CELL ACTIVITY; CELL POPULATION; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; IMAGE DISPLAY; IMAGE PROCESSING; LATENT PERIOD; MALE; MONKEY MODEL; MULTIDIMENSIONAL SCALING; NERVE CELL; NEUROPHYSIOLOGY; NONHUMAN; PULVINAR; SUPERIOR COLLICULUS; VISUAL STIMULATION; VISUAL SYSTEM;

EID: 84896930613     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00085     Document Type: Article

References (94)

1. Arendes, L. (1994). Superior colliculus activity related to attention and to connotative stimulus meaning. Brain Res. Cogn. Brain Res. 2, 65-69. doi: 10.1016/0926-6410(94)90021-3
2. Asahi, T., Tamura, R., Eifuku, S., Hayashi, N., Endo, S., Nishijo, H., et al. (2003). A method for accurate determination of stereotaxic coordinates in single-unit recording studies in monkeys by high-resolution three-dimensional magnetic resonance imaging. Neurosci. Res. 47, 255-260. doi: 10.1016/S0168-0102(03)00202-5
3. Asahi, T., Uwano, T., Eifuku, S., Tamura, R., Endo, S., Ono, T., et al. (2006). Neuronal responses to a delayed-response delayed-reward go/nogo task in the monkey posterior insular cortex. Neuroscience 143, 627-639. doi: 10.1016/j.neuroscience.2006.08.008
4. Barbur, J. L., Ruddock, K. H., and Waterfield, V. A. (1980). Human visual responses in the absence of the geniculo-calcarine projection. Brain 103, 905-928. doi: 10.1093/brain/103.4.905
5. Bell, A. H., Meredith, M. A., Van Opstal, A. J., and Munoz, D. P. (2006). Stimulus intensity modifies saccadic reaction time and visual response latency in the superior colliculus. Exp. Brain Res. 174, 53-59. doi: 10.1007/s00221-006-0420-z
6. Benevento, L. A., and Fallon, J. H. (1975). The ascending projections of the superior colliculus in the rhesus monkey (Macaca mulatta). J. Comp. Neurol. 160, 339-361. doi: 10.1002/cne.901600306
7. Benevento, L. A., and Port, J. D. (1995). Single neurons with both form/color differential responses and saccade-related responses in the nonretinotopic pulvinar of the behaving macaque monkey. Vis. Neurosci. 12, 523-544. doi: 10.1017/S0952523800008439
8. Berman, R. A., and Wurtz, R. H. (2010). Functional identification of a pulvinar path from superior colliculus to cortical area MT. J. Neurosci. 30, 6342-6354. doi: 10.1523/JNEUROSCI.6176-09.2010
9. Berman, R. A., and Wurtz, R. H. (2011). Signals conveyed in the pulvinar pathway from superior colliculus to cortical area MT. J. Neurosci. 31, 373-384. doi: 10.1523/JNEUROSCI.4738-10.2011
10. Bieber, S. L., and Smith, D. V. (1986). Multivariate analysis of sensory data: a comparison of methods. Chem. Sens. 11, 19-47. doi: 10.1093/chemse/11.1.19
11. Blythe, I. M., Kennard, C., and Ruddock, K. H. (1987). Residual vision in patients with retrogeniculate lesions of the visual pathways. Brain 110, 887-905. doi: 10.1093/brain/110.4.887
12. Boehnke, S. E., and Munoz, D. P. (2008). On the importance of the transient visual response in the superior colliculus. Curr. Opin. Neurobiol. 18, 544-551. doi: 10.1016/j.conb.2008.11.004
13. Bruce, C., Desimone, R., and Gross, C. G. (1981). Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J. Neurophysiol. 46, 369-384.
14. Burra, N., Hervais-Adelman, A., Kerzel, D., Tamietto, M., de Gelder, B., and Pegna, A. J. (2013) Amygdala activation for eye contact despite complete cortical blindness. J. Neurosci. 33, 10483-10489. doi: 10.1523/JNEUROSCI.3994-12.2013
15. Carey, S. (1992). Becoming a face expert. Philos. Trans. R. Soc. Lond. B 335, 95-103. doi: 10.1098/rstb.1992.0012
16. Corbetta, M., Miezin, F. M., Dobmeyer, S., Shulman, G. L., and Petersen, S. E. (1991). Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J. Neurosci. 11, 2383-2402.
17. Cynader, M., and Berman, N. (1972). Receptive-field organization of monkey superior colliculus. J. Neurophysiol. 35, 187-201.
18. Day-Brown, J. D., Wei, H., Chomsung, R. D., Petry, H. M., and Bickford, M. E. (2010). Pulvinar projections to the striatum and amygdala in the tree shrew. Front. Neuroanat. 4:143. doi: 10.3389/fnana.2010.00143
19. de Heering, A., Turati, C., Rossion, B., Bulf, H., Goffaux, V., and Simion, F. (2008). Newborns' face recognition is based on spatial frequencies below 0.5 cycles per degree. Cognition 106, 444-454. doi: 10.1016/j.cognition.2006.12.012
20. Desimone, R., Albright, T. D., Gross, C. G., and Bruce, C. (1984). Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051-2062.
21. Doubell, T. P., Skaliora, I., Baron, J., and King, A. J. (2003). Functional connectivity between the superficial and deeper layers of the superior colliculus: an anatomical substrate for sensorimotor integration. J. Neurosci. 23, 6596-6607.
22. Dräger, U. C., and Hubel, D. H. (1976). Topography of visual and somatosensory projections to mouse superior colliculus. J. Neurophysiol. 39, 91-101.
23. Goldberg, M. E., and Wurtz, R. H. (1972). Activity of superior colliculus in behaving monkey. I. Visual receptive fields of single neurons. J. Neurophysiol. 35, 542-559.
24. Grieve, K. L., Acuña, C., and Cudeiro, J. (2000). The primate pulvinar nuclei: vision and action. Trends Neurosci. 23, 35-39. doi: 10.1016/S0166-2236(99)01482-4
25. Grüsser, O. J., and Landis, T. (1991). Visual Agnosia and Other Disturbances of Visual Perception and Cognition. London: MacMillan.
26. Guo, K., Robertson, R. G., Mahmoodi, S., and Young, M. P. (2005). Centre-surround interactions in response to natural scene stimulation in the primary visual cortex. Eur. J. Neurosci. 21, 536-548. doi: 10.1111/j.1460-9568.2005.03858.x
27. Harutiunian-Kozak, B., Dec, K., and Wrobel, A. (1973). The organization of visual receptive fields or neurons in the cat colliculus superior. Acta. Neurobiol. Exp. (Wars) 33, 563-573.
28. Isa, T. (2002). Intrinsic processing in the mammalian superior colliculus. Curr. Opin. Neurobiol. 12, 668-677. doi: 10.1016/S0959-4388(02)00387-2
29. Johnson, M. H. (2005). Subcortical face processing. Nat. Rev. Neurosci. 6, 766-774. doi: 10.1038/nrn1766
30. Johnson, M. H., Dziurawiec, S., Ellis, H., and Morton, J. (1991). Newborns' preferential tracking of face-like stimuli and its subsequent decline. Cognition 40, 1-19. doi: 10.1016/0010-0277(91)90045-6
31. Johnson, M. H., and Horn, G. (1988). Development of filial preferences in dark reared chicks. Anim. Behav. 36, 675-683. doi: 10.1016/S0003-3472(88)80150-7
32. Kaas, J. H., and Lyon, D. C. (2007). Pulvinar contributions to the dorsal and ventral streams of visual processing in primates. Brain Res. Rev. 55, 285-296. doi: 10.1016/j.brainresrev.2007.02.008
33. Kato, R., Takaura, K., Ikeda, T., Yoshida, M., and Isa, T. (2011). Contribution of the retino-tectal pathway to visually guided saccades after lesion of the primary visual cortex in monkeys. Eur. J. Neurosci. 33, 1952-1960. doi: 10.1111/j.1460-9568.2011.07729.x
34. Kruskal, J. B. (1964). Multidimensional scaling by optimizing goodness of fit to a nonmetric hypothesis. Psychometrika 29, 1-27. doi: 10.1007/BF02289565
35. Kusama, T., and Mabuchi, M. (1970). Stereotaxic Atlas of the Brain of Macaca fuscata. Tokyo:: Tokyo University Press.
36. Lamme, V. A., and Roelfsema, P. R. (2000). The distinct modes of vision offered by feedforward and recurrent processing. Trends Neurosci. 23, 571-579. doi: 10.1016/S0166-2236(00)01657-X
37. Leventhal, A. G., Rodieck, R. W., and Dreher, B. (1981). Retinal ganglion cell classes in the Old World monkey: morphology and central projections. Science 213, 1139-1142. doi: 10.1126/science.7268423
38. Li, X., and Basso, M. A. (2008). Preparing to move increases the sensitivity of superior colliculus neurons. J. Neurosci. 28, 4561-4577. doi: 10.1523/JNEUROSCI.5683-07.2008
39. Linke, R., De Lima, A. D., Schwegler, H., and Pape, H. C. (1999). Direct synaptic connections of axons from superior colliculus with identified thalamo-amygdaloid projection neurons in the rat: possible substrates of a subcortical visual pathway to the amygdala. J. Comp. Neurol. 403, 158-170. doi: 10.1002/(SICI)1096-9861(19990111)403:2<158::AID-CNE2>3.0.CO;2-6
40. Maior, R. S., Hori, E., Barros, M., Teixeira, D. S., Tavares, M. C., Ono, T., et al. (2011). Superior colliculus lesions impair threat responsiveness in infant capuchin monkeys. Neurosci. Lett. 504, 257-260. doi: 10.1016/j.neulet.2011.09.042
41. Maior, R. S., Hori, E., Uribe, C. E., Saletti, P. G., Ono, T., Nishijo, H., et al. (2012). A role for the superior colliculus in the modulation of threat responsiveness in primates: towards the ontogenesis of the social brain. Rev. Neurosci. 23, 697-706. doi: 10.1515/revneuro-2012-0055
42. Marino, R. A., Levy, R., Boehnke, S., White, B. J., Itti, L., and Munoz, D. P. (2012). Linking visual response properties in the superior colliculus to saccade behavior. Eur. J. Neurosci. 35, 1738-1752. doi: 10.1111/j.1460-9568.2012.08079.x
43. Matsuda, K. (1996). Measurement system of the eye positions by using oval fitting of a pupil. Neurosci. Res. Suppl. 25, 270. doi: 10.1016/0168-0102(96)89315-1
44. Morland, A. B., Jones, S. R., Finlay, A. L., Deyzac, E., Lê, S., and Kemp, S. (1999). Visual perception of motion, luminance and colour in a human hemianope. Brain 122, 1183-1198. doi: 10.1093/brain/122.6.1183
45. Morris, J. S., DeGelder, B., Weiskrantz, L., and Dolan, R. J. (2001). Differential extrageniculostriate and amygdala responses to presentation of emotional faces in a cortically blind field. Brain 124, 1241-1252. doi: 10.1093/brain/124.6.1241
46. Murray, S. O., Kersten, D., Olshausen, B. A., Schrater, P., and Woods, D. L. (2002). Shape perception reduces activity in human primary visual cortex. Proc. Natl. Acad. Sci. U.S.A. 99, 15164-15169. doi: 10.1073/pnas.192579399
47. Murray, S. O., Schrater, P., and Kersten, D. (2004). Perceptual grouping and the interactions between visual cortical areas. Neural. Netw. 17, 695-705. doi: 10.1016/j.neunet.2004.03.010
48. Nakano, T., Higashida, N., and Kitazawa, S. (2013). Facilitation of face recognition through the retino-tectal pathway. Neuropsychology 51, 2043-2049. doi: 10.1016/j.neuropsychologia.2013.06.018
49. Nguyen, M. N., Hori, E., Matsumoto, J., Tran, A. H., Ono, T., and Nishijo, H. (2013). Neuronal responses to face-like stimuli in the monkey pulvinar. Eur. J. Neurosci. 37, 35-51. doi: 10.1111/ejn.12020
50. Nishijo, H., Kita, T., Tamura, R., Uwano, T., Terasawa, K., and Ono, T. (1997). Septal neuronal responses related to spatial representation in monkeys. Hippocampus 7, 460-464. doi: 10.1002/(SICI)1098-1063(1997)7:5<460::AID-HIPO2>3.0.CO;2-L
51. Nishijo, H., and Norgren, R. (1990). Responses from parabrachial gustatory neurons in behaving rats. J. Neurophysiol. 63, 707-724.
52. Nishijo, H., and Norgren, R. (1991). Parabrachial gustatory neural activity during licking by rats. J. Neurophysiol. 66, 974-985.
53. Nishijo, H., Ono, T., and Nishino, H. (1988a). Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J. Neurosci. 8, 3570-3583.
54. Nishijo, H., Ono, T., and Nishino, H. (1988b). Topographic distribution of modality-specific amygdalar neurons in alert monkey. J. Neurosci. 8, 3556-3569.
55. Scalaidhe, S. P., Wilson, F. A., and Goldman-Rakic, P. S. (1999). Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. Cereb. Cortex 9, 459-475. doi: 10.1093/cercor/9.5.459
56. Panzeri, S., Biella, G., Rolls, E. T., Skaggs, W. E., and Treves, A. (1996). Speed, noise, information and the graded nature of neuronal responses. Network 7, 365-370. doi: 10.1088/0954-898X/7/2/018
57. Perenin, M. T. (1991). Discrimination of motion direction in perimetrically blind fields. Neuroreport 2, 397-400. doi: 10.1097/00001756-199107000-00011
58. Perenin, M. T., and Jeannerod, M. (1975). Residual vision in cortically blind hemiphields. Neuropsychologia 13, 1-7. doi: 10.1016/0028-3932(75)90041-X
59. Perenin, M. T., and Rossetti, Y. (1996). Grasping without form discrimination in a hemianopic field. Neuroreport 7, 793-797. doi: 10.1097/00001756-199602290-00027
60. Perry, V. H., and Cowey, A. (1984). Retinal ganglion cells that project to the superior colliculus and pretectum in the macaque monkey. Neuroscience 12, 1125-1137. doi: 10.1016/0306-4522(84)90007-1
61. Pessoa, L., and Adolphs, R. (2010). Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat. Rev. Neurosci. 11, 773-783. doi: 10.1038/nrn2920
62. Razak, K. A., and Pallas, S. L. (2006). Dark rearing reveals the mechanism underlying stimulus size tuning of superior colliculus neurons. Vis. Neurosci. 23, 741-748. doi: 10.1017/S0952523806230062
63. Rizzolatti, G., Buchtel, H. A., Camarda, R., and Scandolara, C. (1980). Neurons with complex visual properties in the superior colliculus of the macaque monkey. Exp. Brain Res. 38, 37-42. doi: 10.1007/BF00237928
64. Rodieck, R. W., and Watanabe, M. (1993). Survey of the morphology of macaque retinal ganglion cells that project to the pretectum, superior colliculus, and parvicellular laminae of the lateral geniculate nucleus. J. Comp. Neurol. 338, 289-303. doi: 10.1002/cne.903380211
65. Rosa-Salva, O., Farroni, T., Regolin, L., Vallortigara, G., and Johnson, M. H. (2011). The evolution of social orienting: evidence from chicks (Gallus gallus) and human newborns. PLoS ONE 6:e18802. doi: 10.1371/journal.pone.0018802
66. Rosa-Salva, O., Regolin, L., and Vallortigara, G. (2010). Faces are special for newly hatched chicks: evidence for inborn domain-specific mechanisms underlying spontaneous preferences for face-like stimuli. Dev. Sci. 13, 565-577. doi: 10.1111/j.1467-7687.2009.00914.x
67. Sackett, G. P. (1966). Monkeys reared in isolation with pictures as visual input: evidence for an innate releasing mechanism. Science 154, 1468-1473. doi: 10.1126/science.154.3755.1468
68. Sahraie, A., Weiskrantz, L., Trevethan, C. T., Cruce, R., and Murray, A. D. (2002). Psychophysical and pupillometric study of spatial channels of visual processing in blindsight. Exp. Brain Res. 143, 249-256. doi: 10.1007/s00221-001-0989-1
69. Schiller, P. H., and Koerner, F. (1971). Discharge characteristics of single units in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 34, 920-936.
70. Schiller, P. H., and Stryker, M. (1972). Single-unit recording and stimulation in superior colliculus of the alert rhesus monkey. J. Neurophysiol. 35, 915-924.
71. Schmid, M. C., Mrowka, S. W., Turchi, J., Saunders, R. C., Wilke, M., Peters, A. J., et al. (2010). Blindsight depends on the lateral geniculate nucleus. Nature 15, 373-377. doi: 10.1038/nature09179
72. Schmolesky, M. T., Wang, Y., Hanes, D. P., Thompson, K. G., Leutgeb, S., Schall, J. D., et al. (1998). Signal timing across the macaque visual system. J. Neurophysiol. 79, 3272-3278.
73. Schneider, K. A., and Kastner, S. (2005). Visual responses of the human superior colliculus: a high-resolution functional magnetic resonance imaging study. J. Neurophysiol. 94, 2491-2503. doi: 10.1152/jn.00288.2005
74. Serences, J. T., and Yantis, S. (2006). Selective visual attention and perceptual coherence. Trends Cogn. Sci. 10, 38-45. doi: 10.1016/j.tics.2005.11.008
75. Sewards, T. V., and Sewards, M. A. (2002). Innate visual object recognition in vertebrates: some proposed pathways and mechanisms. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 132, 861-891. doi: 10.1016/S1095-6433(02)00119-8
76. Shepard, R. N. (1962). The analysis of proximities: multidimensional scaling with an unknown distance function. Psychometrika 27, 125-140. doi: 10.1007/BF02289630
77. Skaggs, W. E., McNaughton, B. L., Gothard, K. M., and Markus, E. J. (1993). "An information-theoretic approach to deciphering the hippocampal code, " in Advances in Neural Information Processing 5, eds S. J. Hanson, J. D. Cowan, and C. L. Giles (San Mateo, CA: Morgan Kaufmann), 1030-1037.
78. Sparks, D. L. (1986). Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol. Rev. 66, 118-171.
79. Stoerig, P., and Cowey, A. (1997). Blindsight in man and monkey. Brain 120, 535-559. doi: 10.1093/brain/120.3.535
80. Sugita, Y. (2008). Face perception in monkeys reared with no exposure to faces. Proc. Natl. Acad. Sci. U.S.A. 8, 394-398. doi: 10.1073/pnas.0706079105
81. Tamietto, M., and de Gelder, B. (2010). Neural bases of the non-conscious perception of emotional signals. Nat. Rev. Neurosci. 11, 697-709. doi: 10.1038/nrn2889
82. Tazumi, T., Hori, E., Maior, R. S., Ono, T., and Nishijo, H. (2010). Neural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala. Neuroscience 169, 287-301. doi: 10.1016/j.neuroscience.2010.04.028
83. Updyke, B. V. (1974). Characteristics of unit responses in superior colliculus of the Cebus monkey. J. Neurophysiol. 37, 896-909.
84. Van den Stock, J., Tamietto, M., Sorger, B., Pichon, S., Grézes, J., and de Gelder, B. (2011). Cortico-subcortical visual, somatosensory, and motor activations for perceiving dynamic whole-body emotional expressions with and without striate cortex (V1). Proc. Natl. Acad. Sci. U.S.A. 108, 16188-16193. doi: 10.1073/pnas.1107214108
85. Vuilleumier, P. (2000). Faces call for attention: evidence from patients with visual extinction. Neuropsychologia 38, 693-700. doi: 10.1016/S0028-3932(99)00107-4
86. Vuilleumier, P., Armony, J. L., Driver, J., and Dolan, R. J. (2003). Distinct spatial frequency sensitivities for processing faces and emotional expressions. Nat. Neurosci. 6, 624-631. doi: 10.1038/nn1057
87. Wang, L., Sarnaik, R., Rangarajan, K., Liu, X., and Cang, J. (2010). Visual receptive field properties of neurons in the superficial superior colliculus of the mouse. J. Neurosci. 30, 16573-16584. doi: 10.1523/JNEUROSCI.3305-10.2010
88. Weiskrantz, L. (1987). Residual vision in a scotoma-A follow-up study of "form" discrimination. Brain 110, 77-92. doi: 10.1093/brain/110.1.77
89. Weiskrantz, L. (1996). Blindsight revisited. Curr. Opin. Neurobiol. 6, 215-220. doi: 10.1016/S0959-4388(96)80075-4
90. White, B. J., Boehnke, S. E., Marino, R. A., Itti, L., and Munoz, D. P. (2009). Color-related signals in the primate superior colliculus. J. Neurosci. 29, 12159-12166. doi: 10.1523/JNEUROSCI.1986-09.2009
91. Wurtz, R. H., and Mohler, C. W. (1976). Organization of monkey superior colliculus: enhanced visual response of superficial layer cells. J. Neurophysiol. 39, 745-765.
92. Yoshida, M., Itti, L., Berg, D. J., Ikeda, T., Kato, R., Takaura, K., et al. (2012). Residual attention guidance in blindsight monkeys watching complex natural scenes. Curr. Biol. 22, 1429-1434. doi: 10.1016/j.cub.2012.05.046
93. Young, F. W. (1987). Multidimentional Scaling. History, theory, and applications. Hillsdale, NJ: Lawrence Erlbaum.
94. Young, M. P., and Yamane, S. (1992). Sparse population coding of faces in the inferotemporal cortex. Science 256, 1327-1331. doi: 10.1126/science.1598577