Cortical mechanisms of sensory learning and object recognition

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1515, 2009, Pages 321-329

  Hoffman, K L ^a   Logothetis, N K ^b,c  

^a YORK UNIVERSITY   (Canada)

^b MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Amodal perception; Face processing; Invariance; Spike timing

Indexed keywords

COGNITION; LEARNING; NEUROLOGY; PERCEPTION; SENSORY SYSTEM;

EID: 58149234166     PISSN: 09628436     EISSN: None     Source Type: Journal    
DOI: 10.1098/rstb.2008.0271     Document Type: Review

References (89)

1. Afraz, S. R., Kiani, R. & Esteky, H. 2006 Microstimulation of inferotemporal cortex influences face categorization. Nature 442, 692-695.
2. Ahissar, M. & Hochstein, S. 2004 The reverse hierarchy theory of visual perceptual learning. Trends Cogn. Sci. 8, 457-464.
3. Baker, C., Behrmann, M. & Olson, C. R. 2002 Impact of learning on representation of parts and wholes in monkey inferotemporal cortex. Nat. Neurosci. 5, 1210-1216.
4. Biederman, I. 1987 Recognition-by-components: a theory of human image understanding. Psychol. Rev. 94, 115-147.
5. Booth, M. C. A. & Rolls, E. T. 1998 View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. Cereb. Cortex 8, 510-523.
6. Colombo, M. & Gross, C. G. 1994 Responses of inferior temporal cortex and hippocampal neurons during delayed matching to sample in monkeys (Macaca fascicularis). Behav. Neurosci. 108, 443-455.
7. D'Amato, M. R. & Van Sant, P. 1988 The person concept in monkeys (Cebus apella). J. Exp. Psychol. Anim. Behav. Process. 14, 43-55.
8. Dahl, C. D., Logothetis, N. K. & Hoffman, K. L. 2007 Individuation and holistic processing of faces in rhesus monkeys. Proc. R. Soc. B 274, 2069-2076.
9. Davenport, R. K. & Rogers, C. M. 1970 Intermodal equivalence of stimuli in apes. Science 168, 279-280.
10. Desimone, R. & Gross, C. G. 1979 Visual areas in the temporal cortex of the macaque. Brain Res. 178, 363-380.
11. Desimone, R., Albright, T. D., Gross, C. G. & Bruce, C. 1984 Stimulus-selective properties of inferior temporal neurons in the macaque. J. Neurosci. 4, 2051-2062.
12. DiCarlo, J. J. & Maunsell, J.-H. R. 2003 Anterior inferotemporal neurons of monkeys engaged in object recognition can be highly sensitive to object retinal position. J. Neurophysiol. 89, 3264-3278.
13. Eifuku, S., De Souza, W. C., Tamura, R., Nishijo, H. & Ono, T. 2004 Neuronal correlates of face identification in the monkey anterior temporal cortical areas. J. Neurophysiol. 91, 358-371.
14. Elliot, R. C. 1977 Cross-modal recognition in three primates. Neuropsychologia 15, 183-186.
15. Erickson, C. A. & Desimone, R. 1999 Responses of macaque perirhinal neurons during and after visual stimulus association learning. J. Neurosci. 19, 10 404-10 416.
16. Fabre-Thorpe, M., Richard, G. & Thorpe, S. J. 1998 Rapid categorization of natural images by rhesus monkeys. Neuroreport 9, 303-308.
17. Freedman, D. J., Riesenhuber, M., Poggio, T. & Miller, E. K. 2003 A comparison of primate prefrontal and temporal cortices during visual categorization. J. Neurosci. 23, 5235-5246.
18. Freedman, D. J., Riesenhuber, M., Poggio, T. & Miller, E. K. 2006 Experience-dependent sharpening of visual shape selectivity in inferior temporal cortex. Cereb. Cortex 16, 1631-1644.
19. Fukushima, K. 1980 Neocognitron: a self-organizing neural network for a mechanism of pattern recognition unaffected by shift in position. Biol. Cybern. 36, 193-202.
20. Gibson, J. R. & Maunsell, J. H. 1997 Sensory modality specificity of neural activity related to memory in visual cortex. J. Neurophysiol. 78, 1263-1275.
21. Gross, C. G., Rocha-Miranda, C. E. & Bender, D. B. 1972 Visual properties of neurons in inferotemporal cortex of the macaque. J. Neurophysiol. 35, 96-111.
22. Hasselmo, M. E., Rolls, E. T., Baylis, G. C. & Nalwa, V. 1989 Object-centered encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey. Exp. Brain Res. 75, 417-429.
23. Herrnstein, R. J. & Loveland, D. H. 1964 Complex visual concept in the pigeon. Science 146, 549-551.
24. Hoffman, K. L. & Gauthier, I. 2007 Evolutionary specializations for processing faces and objects. In Evolution of nervous systems, vol. 4 (ed. J. H. Kaas), pp. 438-445. Oxford, UK: Elsevier.
25. Hoffman, K. L., Gothard, K. M., Schmid, M. C. & Logothetis, N. K. 2007 Facial-expression and gaze-selective responses in the monkey amygdala. Curr. Biol. 17, 766-772.
26. Horel, J. A. 1993 Retrieval of a face discrimination during suppression of monkey temporal cortex with cold. Neuropsychologia 31, 1067-1077.
27. Horel, J. A. & Misantone, L. J. 1976 Visual discrimination impaired by cutting temporal lobe connections. Science 193, 336-338.
28. Horel, J. A., Pytko-Joiner, D. E., Voytko, M. L. & Salsbury, K. 1987 The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold. Behav. Brain Res. 23, 29-42.
29. Humphrey, N. K. 1974 Species and individuals in the perceptual world of monkeys. Perception 3, 105-114.
30. Hung, C. P., Kreiman, G., Poggio, T. & DiCarlo, J. J. 2005 Fast readout of object indentity from macaque inferior temporal cortex. Science 310, 863-866.
31. Kourtzi, Z. & DiCarlo, J. J. 2006 Learning and neural plasticity in visual object recognition. Curr. Opin. Neurobiol. 16, 152-158.
32. Leopold, D. A., Bondar, I. V. & Giese, M. A. 2006 Norm-based face encoding by single neurons in the monkey inferotemporal cortex. Nature 442, 572-575.
33. Loffler, G., Yourganov, G., Wilkinson, F. & Wilson, H. R. 2005 fMRI evidence for the neural representation of faces. Nat. Neurosci. 8, 1386-1391.
34. Logothetis, N. K. & Pauls, J. 1995 Psychophysical and physiological evidence for viewer-centered object representations in the primate. Cereb. Cortex 5, 270-288.
35. Logothetis, N. K., Pauls, J., Bulthoff, H. H. & Poggio, T. 1994 View-dependent object recognition by monkeys. Curr. Biol. 4, 401-414.
36. Logothetis, N. K., Guggenberger, H., Peled, S. & Pauls, J. 1999 Functional imaging of the monkey brain. Nat. Neurosci. 2, 555-562.
37. Marr, D. 1982 Vision: a computational investigation into the human representation and processing of visual information. San Francisco, CA: Freeman.
38. Martin-Malivel, J. & Fagot, J. 2001 Cross-modal integration and conceptual categorization in baboons. Behav. Brain Res. 122, 209-213.
39. Messinger, A., Squire, L. R., Zola, S. M. & Albright, T. D. 2001 Neuronal representations of stimulus associations develop in the temporal lobe during learning. Proc. Natl Acad. Sci. USA 98, 12 239-12 244.
40. Mishkin, M. 1954 Visual discrimination performance following partial ablations of the temporal lobe. II. Ventral surface vs. hippocampus. J. Comp. Physiol. Psychol. 47, 187-193.
41. Mishkin, M. & Pribram, K. H. 1954 Visual discrimination performance following partial ablations of the temporal lobe. I. Ventral vs. lateral. J. Comp. Physiol. Psychol. 47, 14-20.
42. Miyashita, Y. 1988 Neuronal correlate of visual associative long-term memory in the primate temporal cortex. Nature 335, 817-820.
43. Nielsen, K. J., Logothetis, N. K. & Rainer, G. 2006 Dissociation between local field potentials and spiking activity in macaque inferior temporal cortex reveals diagnosticity-based encoding of complex objects. J. Neurosci. 26, 9639-9645.
44. Op de Beeck, H., Wagemans, J. & Vogels, R. 2001 Inferotemporal neurons represent low-dimensional configurations of parameterized shapes. Nat. Neurosci. 4, 1244-1252.
45. Optican, L. M. & Richmond, B. J. 1987 Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. III. Information theoretic analysis. J. Neurophysiol. 57, 162-178.
46. Oram, M. W. & Perrett, D. I. 1992 Time course of neural responses discriminating different views of the face and head. J. Neurophysiol. 68, 70-84.
47. Pascalis, O. & Bachevalier, J. 1998 Face recognition in primates: a cross-species study. Behav. Process. 43, 87-96.
48. Perrett, D. I. & Oram, M. W. 1993 Neurophysiology of shape processing. Image Vis. Comput. 11, 317-333.
49. Perrett, D. I., Rolls, E. T. & Caan, W. 1982 Visual neurones responsive to faces in the monkey temporal cortex. Exp. Brain Res. 47, 329-342.
50. Pinsk, M. A., DeSimone, K., Moore, T., Gross, C. G. & Kastner, S. 2005 Representations of faces and body parts in macaque temporal cortex: a functional MRI study. Proc. Natl Acad. Sci. USA 102, 6996-7001.
51. Poggio, T. & Edelman, S. 1990 A network that learns to recognize three-dimensional objects. Nature 343, 263-266.
52. Pollen, D. A., Nagler, M., Daugman, J., Kronauer, R. & Cavanagh, P. 1984 Use of gabor elementary functions to probe receptive field substructure of posterior inferotemporal neurons in the owl monkey. Vision Res. 24, 233-241.
53. Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C. & Fried, I. 2005 Invariant visual representation by single neurons in the human brain. Nature 435, 1102-1107.
54. Recanzone, G. H., Merzenich, M. M. & Jenkins, W. M. 1992a Frequency discrimination training engaging a restricted skin surface results in an emergence of a cutaneous response zone in cortical area 3a. J. Neurophysiol. 67, 1057-1070.
55. Recanzone, G. H., Merzenich, M. M. & Schreiner, C. E. 1992b Changes in the distributed temporal response properties of SI cortical neurons reflect improvements in performance on a temporally based tactile discrimination task. J. Neurophysiol. 67, 1071-1091.
56. Recanzone, G. H., Schreiner, C. E. & Merzenich, M. M. 1993 Plasticity in the frequency representation of primary auditory cortex following discrimination training in adult owl monkeys. J. Neurosci. 13, 87-103.
57. Richmond, B. J. & Optican, L. M. 1987 Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. II. Quantification of response waveform. J. Neurophysiol. 57, 147-161.
58. Richmond, B. J., Wurtz, R. H. & Sato, T. 1983 Visual responses of inferior temporal neurons in awake rhesus monkey. J. Neurophysiol. 50, 1415-1432.
59. Richmond, B. J., Optican, L. M., Podell, M. & Spitzer, H. 1987 Temporal encoding of two-dimensional patterns by single units in primate inferior temporal cortex. I. Response characteristics. J. Neurophysiol. 57, 132-146.
60. Roberts, W. A. & Mazmanian, D. S. 1988 Concept learning at different levels of abstraction by pigeons, monkeys, and people. J. Exp. Psychol. Anim. Behav. Process. 14, 247-260.
61. Rolls, E. T. & Baylis, G. C. 1986 Size and contrast have only small effects on the responses to faces of neurons in the cortex of the superior temporal sulcus of the monkey. Exp. Brain Res. 65, 38-48.
62. Rolls, E. T. & Tovee, M. J. 1995 Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J. Neurophysiol. 73, 713-725.
63. Sakai, K. & Miyashita, Y. 1991 Neural organization for the long-term memory of paired associates. Nature 354, 152-155.
64. Sary, G., Vogels, R. & Orban, G. A. 1993 Cue-invariant shape selectivity of macaque inferior temporal neurons. Science 260, 995-997.
65. Sato, T., Kawamura, T. & Iwai, E. 1980 Responsiveness of inferotemporal single units to visual pattern stimuli in monkeys performing discrimination. Exp. Brain Res. 38, 313-319.
66. Schoups, A., Vogels, R., Qian, N. & Orban, G. 2001 Practising orientation identification improves orientation coding in V1 neurons. Nature 412, 549-553.
67. Schrier, A. M. & Brady, P. M. 1987 Categorization of natural stimuli by monkeys (Macaca mulatta): effects of stimulus set size and modification of exemplars. J. Exp. Psychol. Anim. Behav. Process. 13, 136-143.
68. Schrier, A. M., Angarella, R. & Povar, M. L. 1984 Studies of concept formation by stump-tailed monkeys: concepts humans, monkeys, and letter A. J. Exp. Psychol. Anim. Behav. Process. 10, 564-584.
69. Seyfarth, R. M., Cheney, D. L. & Marler, P. 1980 Monkey responses to three different alarm calls: evidence of predator classification and semantic communication. Science 210, 801-803.
70. Sigala, N. & Logothetis, N. K. 2002 Visual categorization shapes feature selectivity in the primate temporal cortex. Nature 415, 318-320.
71. Sigala, N., Gabbiani, F. & Logothetis, N. K. 2002 Visual categorization and object representation in monkeys and humans. J. Cogn. Neurosci. 14, 187-198.
72. Stopfer, M. & Laurent, G. 1999 Short-term memory in olfactory network dynamics. Nature 402, 664-668.
73. Tanaka, J. W. 2001 The entry point of face recognition: evidence for face expertise. J. Exp. Psychol. Gen. 130, 534-543.
74. Thomas, E., Van Hulle, M. M. & Vogels, R. 2001 Encoding of categories by noncategory-specific neurons in the inferior temporal cortex. J. Cogn. Neurosci. 13, 190-200.
75. Tsao, D. Y., Freiwald, W. A., Knutsen, T. A., Mandeville, J. B. & Tootell, R. B. 2003 Faces and objects in macaque cerebral cortex. Nat. Neurosci. 6, 989-995.
76. Ullman, S. 1989 Aligning pictorial descriptions: an approach to object recognition. Cognition 32, 193-254.
77. Ungerleider, L. G. & Mishkin, M. 1982 Two cortical visual systems. In Analysis of visual behavior (eds D. J. Ingle, M. A. Goodale & R. J. W. Mansfield), pp. 549-586. Cambridge, MA: The MIT Press.
78. Vogels, R. 1999 Categorization of complex visual images by rhesus monkeys. Part 2: single-cell study. Eur. J. Neurosci. 11, 1239-1255.
79. Vogels, R. & Orban, G. A. 1994a Activity of inferior temporal neurons during orientation discrimination with successively presented gratings. J. Neurophysiol. 71, 1428-1451.
80. Vogels, R. & Orban, G. A. 1994b Does practice in orientation discrimination lead to changes in the response properties of macaque inferior temporal neurons? Eur. J. Neurosci. 6, 1680-1690.
81. Wallis, G. & Rolls, E. T. 1997 Invariant face and object recognition in the visual system. Prog. Neurobiol. 51, 167-194.
82. Weinberger, N. M. 1993 Learning-induced changes of auditory receptive fields. Curr. Opin. Neurobiol. 3, 570-577.
83. Weiskrantz, L. & Cowey, A. 1975 Cross-modal matching in the rhesus monkey using a single pair of stimuli. Neuropsychologia 13, 257-261.
84. Yamane, S., Kaji, S. & Kawano, K. 1988 What facial features activate face neurons in the inferotemporal cortex of the monkey? Exp. Brain Res. 73, 209-214.
85. Yang, T. & Maunsell, J. H. 2004 The effect of perceptual learning on neuronal responses in monkey visual area V4. J. Neurosci. 24, 1617-1626.
86. Yoshikubo, S. 1985 Species discrimination and concept formation by rhesus monkeys (Macaca mulatta). Primates 26, 285-299.
87. Young, M. P. & Yamane, S. 1992 Sparse population coding of faces in the inferotemporal cortex. Science 256, 1327-1331.
88. Zangenehpour, S. & Chaudhuri, A. 2005 Patchy organization and asymmetric distribution of the neural correlates of face processing in monkey inferotemporal cortex. Curr. Biol. 15, 993-1005.
89. Zohary, E., Celebrini, S., Britten, K. H. & Newsome, W. T. 1994 Neuronal plasticity that underlies improvement in perceptual performance. Science 263, 1289-1292.