Invariant Representations of Objects in Natural Scenes in the Temporal Cortex Visual Areas

  • Edmund T. Rolls


Neurophysiological evidence is described showing that some neurons in the macaque inferior temporal visual cortex have responses that are invariant with respect to the position, size and view of faces and objects, and that these neurons show rapid processing and rapid learning. Which face or object is present is encoded using a distributed representation in which each neuron conveys independent information in its firing rate, with little information evident in the relative time of firing of different neurons. The operation of the inferior temporal cortex when objects are selected in natural scenes, and the encoding of multiple objects in a scene, are described. A theory is described of how such invariant representations may be produced in a hierarchically organized set of visual cortical areas with convergent connectivity. The theory proposes that neurons in these visual areas use a modified Hebb synaptic modification rule with a short term memory trace to capture whatever can be captured at each stage that is invariant about objects as the objects change in retinal view, position, size, and rotation. Another population of neurons in the cortex in the superior temporal sulcus encodes other aspects of faces such as face expression, eye gaze, face view, and whether the head is moving. Outputs of these systems reach the amygdala, in which face-selective neurons are found, and also the orbitofrontal cortex, in which some neurons are tuned to face identity and others to face expression. In humans, activation of the orbitofrontal cortex is found when a change of face expression acts as a social signal that behavior should change; and damage to the orbitofrontal cortex can impair face and voice expression identification, and also the reversal of emotional behavior that normally occurs when reinforcers are reversed (see Rolls, E.T. 2008, Memory, Attention and Decision-Making. Oxford University Press).


Orbitofrontal Cortex Natural Scene Superior Temporal Sulcus Inferior Temporal Cortex Face Expression 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. Abbott LF, Rolls ET, Tovee MJ (1996) Representational capacity of face coding in monkeys. Cereb Cortex 6:498–505PubMedCrossRefGoogle Scholar
  2. Adolphs R, Baron-Cohen S, Tranel D (2002) Impaired recognition of social emotions following amygdala damage. J Cognit Neurosci 14:1264–1274CrossRefGoogle Scholar
  3. Adolphs R, Tranel D, Damasio H, Damasio AR (1995) Fear and the human amygdala. J Neurosci 15:5879–5891PubMedGoogle Scholar
  4. Aggelopoulos NC, Rolls ET (2005) Natural scene perception: inferior temporal cortex neurons encode the positions of different objects in the scene. Eur J Neurosci 22:2903–2916PubMedCrossRefGoogle Scholar
  5. Aggelopoulos NC, Franco L, Rolls ET (2005) Object perception in natural scenes: encoding by inferior temporal cortex simultaneously recorded neurons. J Neurophysiol 93:1342–1357PubMedCrossRefGoogle Scholar
  6. Baddeley RJ, Abbott LF, Booth MJA, Sengpiel F, Freeman T, Wakeman EA, Rolls ET (1997) Responses of neurons in primary and inferior temporal visual cortices to natural scenes. Proc R Soc Lond B 264:1775–1783CrossRefGoogle Scholar
  7. Baizer JS, Ungerleider LG, Desimone R (1991) Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques. J Neurosci 11:168–190PubMedGoogle Scholar
  8. Ballard DH (1990) Animate vision uses object-centred reference frames. In: Eckmiller R (ed) Advanced neural computers. North-Holland, Amsterdam, pp 229–236Google Scholar
  9. Ballard DH (1993) Subsymbolic modelling of hand-eye coordination. In: Broadbent DE (ed) The simulation of human intelligence. Blackwell, Oxford, pp 71–102Google Scholar
  10. Barlow HB (1972) Single units and sensation: a neuron doctrine for perceptual psychology? Perception 1:371–394PubMedCrossRefGoogle Scholar
  11. Baylis GC, Rolls ET (1987) Responses of neurons in the inferior temporal cortex in short term and serial recognition memory tasks. Exp Brain Res 65:614–622PubMedCrossRefGoogle Scholar
  12. Baylis GC, Rolls ET, Leonard CM (1985) Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey. Brain Res 342:91–102PubMedCrossRefGoogle Scholar
  13. Baylis GC, Rolls ET, Leonard CM (1987) Functional subdivisions of the temporal lobe neocortex. J Neurosci 7:330–342PubMedGoogle Scholar
  14. Biederman I (1972) Perceiving real-world scenes. Science 177: 77–80PubMedCrossRefGoogle Scholar
  15. Booth MCA, Rolls ET (1998) View-invariant representations of familiar objects by neurons in the inferior temporal visual cortex. Cereb Cortex 8:510–523PubMedCrossRefGoogle Scholar
  16. Boussaoud D, Desimone R, Ungerleider LG (1991) Visual topography of area TEO in the macaque. J Comp Neurol 306:554–575PubMedCrossRefGoogle Scholar
  17. Brothers L, Ring B, Kling A (1990) Response of neurons in the macaque amygdala to complex social stimuli. Behav Brain Res 41:199–213PubMedCrossRefGoogle Scholar
  18. Bruce C, Desimone R, Gross CG (1981) Visual properties of neurons in a polysensory area in superior temporal sulcus of the macaque. J Neurophysiol 46:369–384PubMedGoogle Scholar
  19. Calder AJ, Young AW, Rowland D, Perrett DI, Hodges JR, Etcoff NL (1996) Facial emotion recognition after bilateral amygdala damage: differentially severe impairment of fear. Cognit Neuropsychol 13:699–745CrossRefGoogle Scholar
  20. Chelazzi L, Miller E, Duncan J, Desimone R (1993) A neural basis for visual search in inferior temporal cortex. Nature (Lond) 363:345–347PubMedCrossRefGoogle Scholar
  21. Corchs S, Deco G (2002) Large-scale neural model for visual attention: integration of experimental single-cell and fMRI data. Cereb Cortex 12:339–348PubMedCrossRefGoogle Scholar
  22. Cowey A, Rolls ET (1975) Human cortical magnification factor and its relation to visual acuity. Exp Brain Res 21:447–454Google Scholar
  23. Deco G, Lee TS (2002) A unified model of spatial and object attention based on intercortical biased competition. Neurocomputing 44–46:769–774Google Scholar
  24. Deco G, Rolls ET (2002) Object-based visual neglect: a computational hypothesis. Eur J Neurosci 16:1994–2000PubMedCrossRefGoogle Scholar
  25. Deco G, Rolls ET (2003) Attention and working memory: a dynamical model of neuronal activity in the prefrontal cortex. Eur J Neurosci 18: 2374–2390PubMedCrossRefGoogle Scholar
  26. Deco G, Rolls ET (2004) A neurodynamical cortical model of visual attention and invariant object recognition. Vision Res 44:621–644PubMedCrossRefGoogle Scholar
  27. Deco G, Rolls ET (2005a) Attention, short-term memory, and action selection: a unifying theory. Prog Neurobiol 76:236–256PubMedGoogle Scholar
  28. Deco G, Rolls ET (2005b) Synaptic and spiking dynamics underlying reward reversal in orbitofrontal cortex. Cereb Cortex 15:15–30PubMedCrossRefGoogle Scholar
  29. Deco G, Rolls ET (2005c) Neurodynamics of biased competition and co-operation for attention: a model with spiking neurons. J Neurophysiol 94:295–313PubMedCrossRefGoogle Scholar
  30. Deco G, Rolls ET (2006) A neurophysiological model of decision-making and Weber’s law. European Journal of Neuroscience 24:901–916PubMedCrossRefGoogle Scholar
  31. Deco G, Zihl J (2001) Top-down selective visual attention: a neurodynamical approach. Visual Cognit 8:119–140Google Scholar
  32. Desimone R (1991) Face-selective cells in the temporal cortex of monkeys. J Cognit Neurosci 3:1–8CrossRefGoogle Scholar
  33. Desimone R, Gross CG (1979) Visual areas in the temporal cortex of the macaque. Brain Res 178:363–380PubMedCrossRefGoogle Scholar
  34. Desimone R, Duncan J (1995) Neural mechanisms of selective visual attention. Annu Rev Neurosci 18:193–222PubMedCrossRefGoogle Scholar
  35. Desimone R, Albright TD, Gross CG, Bruce CJ (1984) Stimulus-selective properties of inferior temporal neurons in the macaque. J Neurosci 4:2051–2062PubMedGoogle Scholar
  36. Dolan RJ, Fink GR, Rolls ET, Booth M, Holmes A, Frackowiak RSJ, Friston KJ (1997) How the brain learns to see objects and faces in an impoverished context. Nature (Lond) 389:596–599PubMedCrossRefGoogle Scholar
  37. Elliffe MCM, Rolls ET, Stringer SM (2002) Invariant recognition of feature combinations in the visual system. Biol Cybern 86:59–71PubMedCrossRefGoogle Scholar
  38. Földiák P (1991) Learning invariance from transformation sequences. Neural Comput 3:194–200CrossRefGoogle Scholar
  39. Franco L, Rolls ET, Aggelopoulos NC, Treves A (2004) The use of decoding to analyze the contribution to the information of the correlations between the firing of simultaneously recorded neurons. Exp Brain Res 155:370–384PubMedCrossRefGoogle Scholar
  40. Franco L, Rolls ET, Aggelopoulos NC, Jerez JM (2007) Neuronal selectivity, population sparseness, and ergodicity in the inferior temporal visual cortex. Biological Cybernetics.Google Scholar
  41. Fukushima K (1980) Neocognitron: a self-organizing neural network model for a mechanism of pattern recognition unaffected by shift in position. Biol Cybern 36:193–202PubMedCrossRefGoogle Scholar
  42. Fukushima K (1989) Analysis of the process of visual pattern recognition by the neocognitron. Neural Networks 2:413–420CrossRefGoogle Scholar
  43. Fukushima K (1991) Neural networks for visual pattern recognition. IEEE Trans 74:179–190Google Scholar
  44. Gawne TJ, Richmond BJ (1993) How independent are the messages carried by adjacent inferior temporal cortical neurons? J Neurosci 13:2758–2771PubMedGoogle Scholar
  45. Georges-François P, Rolls ET, Robertson RG (1999) Spatial view cells in the primate hippocampus: allocentric view not head direction or eye position or place. Cereb Cortex 9:197–212PubMedCrossRefGoogle Scholar
  46. Grill-Spector K, Malach R (2004) The human visual cortex. Annu Rev Neurosci 27:649–677PubMedCrossRefGoogle Scholar
  47. Gross CG, Desimone R, Albright TD, Schwartz EL (1985) Inferior temporal cortex and pattern recognition. Exp Brain Res 11:179–201Google Scholar
  48. Hasselmo ME, Rolls ET, Baylis GC (1989a) The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav Brain Res 32:203–218PubMedCrossRefGoogle Scholar
  49. Hasselmo ME, Rolls ET, Baylis GC, Nalwa V (1989b) Object-centred encoding by face-selective neurons in the cortex in the superior temporal sulcus of the monkey. Exp Brain Res 75:417–429PubMedCrossRefGoogle Scholar
  50. Haxby JV, Hoffman EA, Gobbini MI (2002) Human neural systems for face recognition and social communication. Biol Psychiatry 51:59–67PubMedCrossRefGoogle Scholar
  51. Hornak J, Rolls ET, Wade D (1996) Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage. Neuropsychologia 34:247–261PubMedCrossRefGoogle Scholar
  52. Hornak J, Bramham J, Rolls ET, Morris RG, O’Doherty J, Bullock PR, Polkey CE (2003) Changes in emotion after circumscribed surgical lesions of the orbitofrontal and cingulated cortices. Brain 126:1691–1712PubMedCrossRefGoogle Scholar
  53. Hornak J, O’Doherty J, Bramham J, Rolls ET, Morris RG, Bullock PR, Polkey CE (2004) Reward-related reversal learning after surgical excisions in orbitofrontal and dorsolateral prefrontal cortex in humans. J Cognit Neurosci 16:463–478CrossRefGoogle Scholar
  54. Koenderink JJ, Van Doorn AJ (1979) The internal representation of solid shape with respect to vision. Biol Cybern 32:211–217PubMedCrossRefGoogle Scholar
  55. Kringelbach ML, Rolls ET (2003) Neural correlates of rapid reversal learning in a simple model of human social interaction. Neuroimage 20:1371–1383PubMedCrossRefGoogle Scholar
  56. Kringelbach ML, Rolls ET (2004) The functional neuroanatomy of the human orbitofrontal cortex: evidence from neuroimaging and neuropsychology. Prog Neurobiol 72:341–372PubMedCrossRefGoogle Scholar
  57. Leonard CM, Rolls ET, Wilson FAW, Baylis GC (1985) Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 15:159–176PubMedCrossRefGoogle Scholar
  58. Logothetis NK, Sheinberg DL (1996) Visual object recognition. Annu Rev Neurosci 19:577–621PubMedCrossRefGoogle Scholar
  59. Logothetis NK, Pauls J, Bülthoff HH, Poggio T (1994) View-dependent object recognition by monkeys. Curr Biol 4:401–414PubMedCrossRefGoogle Scholar
  60. Marr D (1982) Vision. Freeman, San FranciscoGoogle Scholar
  61. Martinez-Trujillo J, Treue S (2002) Attentional modulation strength in cortical area MT depends on stimulus contrast. Neuron 35:365–370PubMedCrossRefGoogle Scholar
  62. Maunsell JH, Newsome WT (1987) Visual processing in monkey extrastriate cortex. Annu Rev Neurosci 10:363–401PubMedCrossRefGoogle Scholar
  63. Mikami A, Nakamura K, Kubota K (1994) Neuronal responses to photographs in the superior temporal sulcus of the rhesus monkey. Behav Brain Res 60:1–13PubMedCrossRefGoogle Scholar
  64. Miller EK, Desimone R (1994) Parallel neuronal mechanisms for short-term memory. Science 263:520–522PubMedCrossRefGoogle Scholar
  65. Miyashita Y (1993) Inferior temporal cortex: where visual perception meets memory. Annu Rev Neurosci 16:245–263PubMedCrossRefGoogle Scholar
  66. Mozer M (1991) The perception of multiple objects: a connectionist approach. MIT Press, CambridgeGoogle Scholar
  67. Panzeri S, Biella G, Rolls ET, Skaggs WE, Treves A (1996) Speed, noise, information and the graded nature of neuronal responses. Network 7:365–370PubMedGoogle Scholar
  68. Panzeri S, Treves A, Schultz S, Rolls ET (1999a) On decoding the responses of a population of neurons from short time epochs. Neural Comput 11:1553–1577PubMedCrossRefGoogle Scholar
  69. Panzeri S, Schultz SR, Treves A, Rolls ET (1999b) Correlations and the encoding of information in the nervous system. Proc R Soc Lond B 266:1001–1012CrossRefGoogle Scholar
  70. Panzeri S, Rolls ET, Battaglia F, Lavis R (2001) Speed of feed-forward and recurrent processing in multilayer networks of integrate-and-fire neurons. Network Comput Neural Syst 12:423–440CrossRefGoogle Scholar
  71. Perrett DI, Rolls ET, Caan W (1982) Visual neurons responsive to faces in the monkey temporal cortex. Exp Brain Res 47:329–342PubMedCrossRefGoogle Scholar
  72. Perrett DI, Smith PA, Potter DD, Mistlin AJ, Head AS, Milner AD, Jeeves MA (1985a) Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B 223:293–317PubMedCrossRefGoogle Scholar
  73. Perrett DI, Smith PAJ, Mistlin AJ, Chitty AJ, Head AS, Potter DD, Broennimann R, Milner AD, Jeeves MA (1985b) Visual analysis of body movements by neurons in the temp oral cortex of the macaque monkey: a preliminary report. Behav Brain Res 16:153–170PubMedCrossRefGoogle Scholar
  74. Perrett D, Mistlin A, Chitty A (1987) Visual neurons responsive to faces. Trends Neurosci 10:358–364CrossRefGoogle Scholar
  75. Phelps EA (2004) Human emotion and memory: interactions of the amygdala and hippocampal complex. Curr Opin Neurobiol 14:198–202PubMedCrossRefGoogle Scholar
  76. Poggio T, Edelman S (1990) A network that learns to recognize three-dimensional objects. Nature (Lond) 343:263–266PubMedCrossRefGoogle Scholar
  77. Renart A, Parga N, Rolls ET (2000) A recurrent model of the interaction between the prefrontal cortex and inferior temporal cortex in delay memory tasks. In: Solla SA, Leen TK, Mueller KR (eds) Advances in neural information processing systems, vol 12. MIT Press, Cambridge, pp 171–177Google Scholar
  78. Renart A, Moreno R, de la Rocha J, Parga N, Rolls ET (2001) A model of the IT-PF network in object working memory which includes balanced persistent activity and tuned inhibition. Neurocomputing 38–40:1525–1531CrossRefGoogle Scholar
  79. Reynolds J, Desimone R (1999) The role of neural mechanisms of attention in solving the binding problem. Neuron 24:19–29PubMedCrossRefGoogle Scholar
  80. Reynolds JH, Chelazzi L, Desimone R (1999) Competitive mechanisms subserve attention in macaque areas V2 and V4. J Neurosci 19:1736–1753PubMedGoogle Scholar
  81. Robertson RG, Rolls ET, Georges-François P (1998) Spatial view cells in the primate hippocampus: effects of removal of view details. J Neurophysiol 79:1145–1156PubMedGoogle Scholar
  82. Rolls ET (1981) Responses of amygdaloid neurons in the primate. In: Ben-Ari Y (ed) The amygdaloid complex. Elsevier, Amsterdam, pp 383–393Google Scholar
  83. Rolls ET (1984) Neurons in the cortex of the temporal lobe and in the amygdala of the monkey with responses selective for faces. Human Neurobiol 3:209–222Google Scholar
  84. Rolls ET (1986a) A theory of emotion, and its application to understanding the neural basis of emotion. In: Oomura Y (ed) Emotions. Neural and chemical control. Karger, Basel, pp 325–344Google Scholar
  85. Rolls ET (1986b) Neural systems involved in emotion in primates. In: Plutchik R, Kellerman H (eds) Emotion: theory, research, and experience, vol 3. Biological foundations of emotion. Academic Press, New York, pp 125–143Google Scholar
  86. Rolls ET (1989a) Functions of neuronal networks in the hippocampus and neocortex in memory. In: Byrne JH, Berry WO (eds) Neural models of plasticity: experimental and theoretical approaches. Academic Press, San Diego, pp 240–265Google Scholar
  87. Rolls ET (1989b) The representation and storage of information in neuronal networks in the primate cerebral cortex and hippocampus. In: Durbin R, Miall C, Mitchison G (eds) The computing neuron. Addison-Wesley, Wokingham, England, pp 125–159Google Scholar
  88. Rolls ET (1990) A theory of emotion, and its application to understanding the neural basis of emotion. Cognit Emotion 4:161–190CrossRefGoogle Scholar
  89. Rolls ET (1991) Neural organisation of higher visual functions. Curr Opin Neurobiol 1:274–278PubMedCrossRefGoogle Scholar
  90. Rolls ET (1992a) Neurophysiological mechanisms underlying face processing within and beyond the temporal cortical visual areas. Philos Trans R Soc Lond B 335:11–21CrossRefGoogle Scholar
  91. Rolls ET (1992b) Neurophysiology and functions of the primate amygdala. In: Aggleton JP (ed) The amygdala. Wiley-Liss, New York, pp 143–165Google Scholar
  92. Rolls ET (1997) A neurophysiological and computational approach to the functions of the temporal lobe cortical visual areas in invariant object recognition. In: Jenkin M, Harris L (eds) Computational and psychophysical mechanisms of visual coding. Cambridge University Press, Cambridge, pp 184–220Google Scholar
  93. Rolls ET (1999a) The functions of the orbitofrontal cortex. Neurocase 5:301–312CrossRefGoogle Scholar
  94. Rolls ET (1999b) The brain and emotion. Oxford University Press, OxfordGoogle Scholar
  95. Rolls ET (1999c) Spatial view cells and the representation of place in the primate hippocampus. Hippocampus 9:467–480PubMedCrossRefGoogle Scholar
  96. Rolls ET (2000a) Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition. Neuron 27:205–218PubMedCrossRefGoogle Scholar
  97. Rolls ET (2000b) Neurophysiology and functions of the primate amygdala, and the neural basis of emotion. In: Aggleton JP (ed) The amygdala: a functional analysis, 2nd edn. Oxford University Press, Oxford, pp 447–478Google Scholar
  98. Rolls ET (2003) Consciousness absent and present: a neurophysiological exploration. Prog Brain Res 144:95–106CrossRefGoogle Scholar
  99. Rolls ET (2005) Emotion explained. Oxford University Press, OxfordGoogle Scholar
  100. Rolls ET (2007) The representation of information about faces in the temporal and frontal lobes. Neuropsychologia 45:124–143PubMedCrossRefGoogle Scholar
  101. Rolls ET (2008) Memory, attention, and decision-making. Oxford University Press, OxfordGoogle Scholar
  102. Rolls ET, Baylis GC (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 65:38–48PubMedCrossRefGoogle Scholar
  103. Rolls ET, Cowey A (1970) Topography of the retina and striate cortex and its relationship to visual acuity in rhesus monkeys and squirrel monkeys. Exp Brain Res 10:298–310PubMedCrossRefGoogle Scholar
  104. Rolls ET, Deco G (2002) Computational neuroscience of vision. Oxford University Press, OxfordGoogle Scholar
  105. Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Progress in Neurobiology 79:1–48PubMedCrossRefGoogle Scholar
  106. Rolls ET, Milward T (2000) A model of invariant object recognition in the visual system: learning rules, activation functions, lateral inhibition, and information-based performance measures. Neural Comput 12:2547–2572PubMedCrossRefGoogle Scholar
  107. Rolls ET, Stringer SM (2001) Invariant object recognition in the visual system with error correction and temporal difference learning. Network Comput Neural Syst 12:111–129CrossRefGoogle Scholar
  108. Rolls ET, Stringer SM (2006) Invariant visual object recognition: a model, with lighting invariance. Journal of Physiology — Paris 100:43–62CrossRefGoogle Scholar
  109. Rolls ET, Stringer SM (2007) Invariant global motion recognition in the dorsal visual system: a unifying theory. Neural Computation 19:139–169PubMedCrossRefGoogle Scholar
  110. Rolls ET, Tovee MJ (1994) Processing speed in the cerebral cortex and the neurophysiology of visual masking. Proc R Soc Lond B 257:9–15CrossRefGoogle Scholar
  111. Rolls ET, Tovee MJ (1995a) Sparseness of the neuronal representation of stimuli in the primate temporal visual cortex. J Neurophysiol 73:713–726PubMedGoogle Scholar
  112. Rolls ET, Tovee MJ (1995b) The responses of single neurons in the temporal visual cortical areas of the macaque when more than one stimulus is present in the visual field. Exp Brain Res 103:409–420PubMedCrossRefGoogle Scholar
  113. Rolls ET, Treves A (1990) The relative advantages of sparse versus distributed encoding for associative neuronal networks in the brain. Network 1:407–421CrossRefGoogle Scholar
  114. Rolls ET, Treves A (1998) Neural networks and brain function. Oxford University Press, OxfordGoogle Scholar
  115. Rolls ET, Xiang J-Z (2005) Reward-spatial view representations and learning in the hippocampus. J Neurosci 25:6167–6174PubMedCrossRefGoogle Scholar
  116. Rolls ET, Xiang J-Z (2006) Spatial view cells in the primate hippocampus, and memory recall. Rev Neurosci 17:175–200PubMedGoogle Scholar
  117. Rolls ET, Baylis GC, Leonard CM (1985) Role of low and high spatial frequencies in the face-selective responses of neurons in the cortex in the superior temporal sulcus in the monkey. Vision Res 25:1021–1035PubMedCrossRefGoogle Scholar
  118. Rolls ET, Baylis GC, Hasselmo ME (1987) The responses of neurons in the cortex in the superior temporal sulcus of the monkey to band-pass spatial frequency filtered faces. Vision Res 27:311–326PubMedCrossRefGoogle Scholar
  119. Rolls ET, Baylis GC, Hasselmo M, Nalwa V (1989a) The representation of information in the temporal lobe visual cortical areas of macaque monkeys. In: Kulikowski JJ, Dickinson CM, Murray IJ (eds) Seeing contour and colour. Pergamon, OxfordGoogle Scholar
  120. Rolls ET, Baylis GC, Hasselmo ME, Nalwa V (1989b) The effect of learning on the face selective responses of neurons in the cortex in the superior temporal sulcus of the monkey. Exp Brain Res 76:153–164PubMedCrossRefGoogle Scholar
  121. Rolls ET, Tovee MJ, Purcell DG, Stewart AL, Azzopardi P (1994) The responses of neurons in the temporal cortex of primates, and face identification and detection. Exp Brain Res 101:473–484PubMedCrossRefGoogle Scholar
  122. Rolls ET, Critchley HD, Treves A (1996) The representation of olfactory information in the primate orbitofrontal cortex. J Neurophysiol 75:1982–1996PubMedGoogle Scholar
  123. Rolls ET, Treves A, Tovee MJ (1997a) The representational capacity of the distributed encoding of information provided by populations of neurons in the primate temporal visual cortex. Exp Brain Res 114:177–185CrossRefGoogle Scholar
  124. Rolls ET, Robertson RG, Georges-François P (1997b) Spatial view cells in the primate hippocampus. Eur J Neurosci 9:1789–1794PubMedCrossRefGoogle Scholar
  125. Rolls ET, Treves A, Robertson RG, Georges-François P, Panzeri S (1998) Information about spatial view in an ensemble of primate hippocampal cells. J Neurophysiol 79:1797–1813PubMedGoogle Scholar
  126. Rolls ET, Tovee MJ, Panzeri S (1999) The neurophysiology of backward visual masking: information analysis. J Cognit Neurosci 11:335–346CrossRefGoogle Scholar
  127. Rolls ET, Aggelopoulos NC, Zheng F (2003a) The receptive fields of inferior temporal cortex neurons in natural scenes. J Neurosci 23:339–348PubMedGoogle Scholar
  128. Rolls ET, Franco L, Aggelopoulos NC, Reece S (2003b) An information theoretic approach to the contributions of the firing rates and correlations between the firing of neurons. J Neurophysiol 89:2810–2822PubMedCrossRefGoogle Scholar
  129. Rolls ET, Aggelopoulos NC, Franco L, Treves A (2004) Information encoding in the inferior temporal cortex: contributions of the firing rates and correlations between the firing of neurons. Biol Cybern 90:19–32PubMedCrossRefGoogle Scholar
  130. Rolls ET, Xiang J-Z, Franco L (2005) Object, space and object-space representations in the primate hippocampus. J Neurophysiol 94:833–844PubMedCrossRefGoogle Scholar
  131. Rolls ET, Critchley HD, Browning AS, Inoue K (2006a) Face-selective and auditory neurons in the primate orbitofrontal cortex. Exp Brain Res 170:74–87PubMedCrossRefGoogle Scholar
  132. Rolls ET, Franco L, Aggelopoulos NC, Perez JM (2006b) Information in the first spike, the order of spikes, and the number of spikes provided by neurons in the inferior temporal visual cortex. Vision Res 46:4193–4205PubMedCrossRefGoogle Scholar
  133. Sato T (1989) Interactions of visual stimuli in the receptive fields of inferior temporal neurons in awake macaques. Exp Brain Res 77:23–30PubMedCrossRefGoogle Scholar
  134. Seltzer B, Pandya DN (1978) Afferent cortical connections and architectonics of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Res 149:1–24PubMedCrossRefGoogle Scholar
  135. Singer W (1999) Neuronal synchrony: a versatile code for the definition of relations? Neuron 24:49–65PubMedCrossRefGoogle Scholar
  136. Singer W, Gray CM (1995) Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 18:555–586PubMedCrossRefGoogle Scholar
  137. Spiridon M, Kanwisher N (2002) How distributed is visual category information in human occipito-temporal cortex? An fMRI study. Neuron 35:1157–1165PubMedCrossRefGoogle Scholar
  138. Stringer SM, Rolls ET (2000) Position invariant recognition in the visual system with cluttered environments. Neural Networks 13:305–315PubMedCrossRefGoogle Scholar
  139. Stringer SM, Rolls ET (2002) Invariant object recognition in the visual system with novel views of 3D objects. Neural Comput 14:2585–2596PubMedCrossRefGoogle Scholar
  140. Stringer SM, Perry G, Rolls ET, Proske JH (2006) Learning invariant object recognition in the visual system with continuous transformations. Biol Cybern 94:128–142PubMedCrossRefGoogle Scholar
  141. Sutton RS, Barto AG (1998) Reinforcement learning. MIT Press, CambridgeGoogle Scholar
  142. Tanaka K (1993) Neuronal mechanisms of object recognition. Science 262:685–688PubMedCrossRefGoogle Scholar
  143. Tanaka K (1996) Inferotemporal cortex and object vision. Annu Rev Neurosci 19:109–139PubMedCrossRefGoogle Scholar
  144. Tanaka K, Saito C, Fukada Y, Moriya M (1990) Integration of form, texture, and color information in the inferotemporal cortex of the macaque. In: Iwai E, Mishkin M (eds) Vision, memory and the temporal lobe. Elsevier, New York, pp 101–109.Google Scholar
  145. Thorpe SJ, Imbert M (1989) Biological constraints on connectionist models. In: Pfeifer R, Schreter Z, Fogelman-Soulie F (eds) Connectionism in perspective. Elsevier, Amsterdam, pp 63–92Google Scholar
  146. Thorpe SJ, Rolls ET, Maddison S (1983) Neuronal activity in the orbitofrontal cortex of the behaving monkey. Exp Brain Res 49:93–115PubMedCrossRefGoogle Scholar
  147. Tovee MJ, Rolls ET (1995) Information encoding in short firing rate epochs by single neurons in the primate temporal visual cortex. Visual Cognit 2:35–58CrossRefGoogle Scholar
  148. Tovee MJ, Rolls ET, Treves A, Bellis RP (1993) Information encoding and the responses of single neurons in the primate temporal visual cortex. J Neurophysiol 70:640–654PubMedGoogle Scholar
  149. Tovee MJ, Rolls ET, Azzopardi P (1994) Translation invariance in the responses to faces of single neurons in the temporal visual cortical areas of the alert macaque. J Neurophysiol 72:1049–1060PubMedGoogle Scholar
  150. Tovee MJ, Rolls ET, Ramachandran VS (1996) Rapid visual learning in neurones of the primate temporal visual cortex. Neuroreport 7:2757–2760PubMedCrossRefGoogle Scholar
  151. Trappenberg TP, Rolls ET, Stringer SM (2002) Effective size of receptive fields of inferior temporal cortex neurons in natural scenes. In: Dietterich TG, Becker S, Ghahramani Z (eds) Advances in neural information processing systems, 14, vol 1. MIT Press, Cambridge, pp 293–300Google Scholar
  152. Treves A (1993) Mean-field analysis of neuronal spike dynamics. Network 4:259–284Google Scholar
  153. Treves A, Rolls ET (1991) What determines the capacity of autoassociative memories in the brain? Network 2:371–397Google Scholar
  154. Treves A, Rolls ET, Tovee MJ (1996) On the time required for recurrent processing in the brain. In: Torre V, Conti F (eds) Neurobiology: ionic channels, neurons, and the brain. Plenum, New York, pp 325–353Google Scholar
  155. Treves A, Rolls ET, Simmen M (1997) Time for retrieval in recurrent associative memories. Physica D 107:392–400CrossRefGoogle Scholar
  156. Treves A, Panzeri S, Rolls ET, Booth M, Wakeman EA (1999) Firing rate distributions and efficiency of information transmission of inferior temporal cortex neurons to natural visual stimuli. Neural Computat 11:611–641CrossRefGoogle Scholar
  157. Ullman S (1996) High-level vision: object recognition and visual cognition. Bradford/MIT Press, CambridgeGoogle Scholar
  158. Usher M, Niebur E (1996) Modelling the temporal dynamics of IT neurons in visual search: a mechanism for top-down selective attention. J Cognit Neurosci 8:311–327CrossRefGoogle Scholar
  159. von der Malsburg C (1990) A neural architecture for the representation of scenes. In: McGaugh JL, Weinberger NM, Lynch G (eds) Brain organisation and memory: cells, systems and circuits. Oxford University Press, New York, pp 356–372Google Scholar
  160. Wallis G, Rolls ET (1997) Invariant face and object recognition in the visual system. Prog Neurobiol 51:167–194PubMedCrossRefGoogle Scholar
  161. Wallis G, Rolls ET, Földiák P (1993) Learning invariant responses to the natural transformations of objects. In: International Joint Conference on Neural Networks, vol 2, pp 1087–1090Google Scholar
  162. Williams GV, Rolls ET, Leonard CM, Stern C (1993) Neuronal responses in the ventral striatum of the behaving macaque. Behav Brain Res 55:243–252PubMedCrossRefGoogle Scholar
  163. Wilson FAW, O’Scalaidhe SPO, Goldman-Rakic PS (1993) Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 260:1955–1958PubMedCrossRefGoogle Scholar
  164. Xiang J-Z, Brown MW (1998) Differential neuronal encoding of novelty, familiarity and recency in regions of the anterior temporal lobe. Neuropharmacology 37:657–676PubMedCrossRefGoogle Scholar
  165. Yamane S, Kaji S, Kawano K (1988) What facial features activate face neurons in the inferotemporal cortex of the monkey? Exp Brain Res 73:209–214PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • Edmund T. Rolls
    • 1
  1. 1.Department of Experimental PsychologyUniversity of OxfordOxfordUK

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