Is right hemisphere specialization for face discrimination specific to humans?

European Journal of Neuroscience

Volumn 12, Issue 2, 2000, Pages 731-741

  Broad, Kevin D ^b   Mimmack, Michael L ^a   Kendrick, Keith M ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

c fos; Face recognition; Hemispheric lateralization (asymmetry); Sheep; Temporal cortex; zif 268

Indexed keywords

PROTEIN C FOS;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN ASYMMETRY; CINGULATE GYRUS; CONTROLLED STUDY; FACE; HIPPOCAMPUS; NONHUMAN; OPTICAL DENSITY; PARIETAL LOBE; PRIORITY JOURNAL; RECOGNITION; RIGHT HEMISPHERE; SHEEP; TEMPORAL CORTEX; VISUAL DISCRIMINATION;

AMYGDALA; ANIMALS; DISCRIMINATION (PSYCHOLOGY); DOMINANCE, CEREBRAL; FACE; GENE EXPRESSION REGULATION; GENES, FOS; HIPPOCAMPUS; HUMANS; MAZE LEARNING; MEMORY; NERVE TISSUE PROTEINS; PARIETAL LOBE; PATTERN RECOGNITION, VISUAL; PREFRONTAL CORTEX; PROTO-ONCOGENE PROTEINS C-FOS; RNA, MESSENGER; SHEEP; SPECIES SPECIFICITY; TEMPORAL LOBE;

EID: 0034050731     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.2000.00934.x     Document Type: Article

References (90)

1. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. (1994). Impaired recognition of emotion in facial expressions following bilateral damage to the human amygdala. Nature., 372, 669-672.
2. Adolphs, R., Tranel, D., Damasio, H. & Damasio, A. (1995). Fear and the human amygdala. J. Neurosci., 15, 5879-5891.
3. Amaral, D.G., Price, J.L., Pitk'anen, A. & Carmichael, S.T. (1992). Anatomical organisation of the primate amygdaloid complex. In Aggleton, J.P. (ed.), The Amygdala: Neurobiological Aspects of Emotion, Memory, and Mental Dysfunction. Wiley-Liss, New York, pp. 1-66.
4. Bauer, R.H. (1993). Lateralisation of neural control for vocalisation by the frog (Rana pipiens). Psychobiology, 21, 243-248.
5. Bigl, V., Woolf, N.J. & Butcher, L.L. (1982). Cholinergic projections from the basal forebrain to frontal, parietal, temporal, occipital and cingulate cortices: a combined fluorescent tracer and acetylcholinesterase analysis. Brain Res. Bull., 8, 727-749.
6. Bradshaw, J.L. & Rogers, L.J. (1993). The Evolution of Lateral Asymmetries, Langauge, Tool Use and Intellect. Academic Press, San Diego.
7. Broad, K.D. Whelan-Buckley, A. Wilkinson, L.S. Keverne, E.B. & Kendrick, K.M. (1998). The medial frontal cortex is involved in mediating executive motor responses to olfactory cues rather than olfactory memory formation. Soc. Neurosci. Abstr., 24, 662.5.
8. Broman, M. (1978). Reaction time differences between left and right hemispheres for face and letter discrimination in children and adults. Cortex, 14, 578-591.
9. Bussey, T.J., Muir, J.L., Everitt, B.J. & Robbins, T.W. (1996). Dissociable effects of anterior cingulate, posterior cingulate cortex lesions on the acquisition of a conditional visual discrimination: facilitation of early learning vs. impairment of late learning. Behav. Brain Res., 82, 45-56.
10. Bussey, T.J., Muir, J.L., Everitt, B.J. & Robbins, T.W. (1997a). Triple dissociation of anterior cingulate, posterior cingulate and medial frontal cortices on visual discrimination tasks using a touch screen testing procedure for the rat. Behav. Neurosci, 111, 920-936.
11. Bussey, T.J., Everitt, B.J. & Robbins, T.W. (1997b). Dissociable effects of cingulate and medial frontal cortex lesions on stimulus-reward learning using a novel Pavlovian autoshaping procedure for the rat: implications for the neurobiology of emotion, Behav. Neurosci, 111, 908-919.
12. Cantalupo, C. & Bisazza, A. & Vallortigara, G. (1996). Lateralisation of displays during aggressive and courtship behaviour in the Siamese fighting fish (Betta splendens). Physiol. Behav., 60, 249-252.
13. Carlson, S. & Goldman-Rakic, P. (1995). Dissociation of movement related neuronal activity in the posterior cingulate cortex in monkeys performing oculomotor and manual delayed response tasks. Soc. Neurosci. Abstr., 21, 1929.
14. Changelian, P.S., Feng, P., King, T.C. & Milbrandt, J. (1989). Structure of the NGFlα gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor. Proc. Natl Acad. Sci. USA, 86, 377-381.
15. Chavis, D.A. & Pandya, D.N. (1976). Further observation on cortico-frontal connections in the rhesus monkey. Brain Res., 117, 369-386.
16. Colby, C.L. & Duhamel, J.R. (1996). Spatial representations for action in the parietal cortex. Cognit. Brain Res., 5, 105-117.
17. Corbetta, M., Miezin, F.M., Dobmer, S., Shulman, G.L. & Petersen, S.E. (1991). Selective and divided attention during visual discrimination of shape, colour and speed: functional anatomy by positron emission tomography. J. Neurosci., 11, 2382-2402.
18. Courtney, S.M., Ungerleider, L.G., Keil, K. & Haxby, J.V. (1996). Object and spatial visual working memory activate separate neural systems in human cortex. Cerebral Cortex, 6, 39-49.
19. Cummings, J.L. (1995). Anatomic and behavioural aspects of frontal subcortical circuits. Ann. NY Acad. Sci., 769, 1-13.
20. Cynx, J., Williams, H. & Nottebohm, F. (1992). Hemispheric differences in avian song discrimination. Proc. Natl Acad. Sci. USA., 89, 1372-1375.
21. da Costa, A.P.C., Broad, K.D. & Kendrick, K.M. (1997). Olfactory memory and maternal behaviour-induced changes in c-fos and zifl268 mRNA expression in the sheep brain. Mol. Brain Res., 46, 63-76.
22. Damasio, A.R., Damasio, H. & van Hoesen, G.W. (1982). Prosopagnosia - anatomic basis and behavioural mechanisms. Neurology, 32, 331-341.
23. De Renzi, E., Perani, D., Carlesimo, G.A., Silveri, M.C. & Facio, F. (1994). Prosopagnosia can be associated with damage confined to the right hemisphere: an MRI and PET study and a review of the literature. Neuropsychologia, 179, 893-902.
24. Diamond, R. & Carey, S. (1986). Why faces are and are not special: an effect of expertise. J. Exp. Psychol: Gen., 155, 107-117.
25. Egly, R., Driver, J. & Rafal, R.D. (1994). Shifting visual attention between objects and locations: evidence from normal and parietal lesioned subjects. J. Exp. Psychol. Gen., 123, 161-177.
26. Evans, J.J., Heggs, A.J., Antoun, N. & Hodges, J.R. (1995). Progressive prosopagnosia associated with selective right temporal lobe atrophy. A new syndrome? Brain, 118, 1-13.
27. Fried, I., MacDonald, K.A. & Wilson, C.L. (1997) Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron, 18, 753-763.
28. Friedman-Hill, S.R., Robertson, L.C. & Triesman, A. (1995). Parietal contributions to visual feature binding: evidence from a patient with bilateral lesions. Science, 269, 853-855.
29. Gabriel, M. (1993). Discriminative avoidance learning a model system. In Vogt, B.A. & Gabriel, M. (eds), Neurobiology of Cingulate Cortex and Limbic Thalamus: a Comprehensive Handbook. Birkhäuser, Boston, pp. 478-523.
30. Gannon, P.J., Holloway, R.L., Broadfield, D.C. & Braun, A.R. (1998). Asymetry of chimpanzee planum temporale: humanlike pattern of Wernicke's brain language area homolog. Science, 279 (5378), 220-222.
31. Gilbert, G. & Bakan, P. (1973) Visual asymmetry in the perception of faces. Neuropsychologica, 31, 609-619.
32. Gross, C.G., Rocha-Miranda, C.E. & Bender, D.B. (1972). Visual properties of neurons in the inferotemporal cortex of the macaque. J. Neurophysiol., 35, 96-111.
33. Gur, R.C., Ragland, J.D., Mozley, L.H., Mozley, P.D., Smith, R., Alavi, A., Bilker, W. & Gur, R.E. (1997). Lateralised changes in regional cerebral blood flow during performance of verbal and facial recognition tasks: correlations with performance and 'Effort'. Brain Cognit., 33, 388-414.
34. Hamilton, C.R. (1977). An assesment of hemispheric specialisation in monkeys. Ann. NY Acad. Sci., 299, 222-232.
35. Hamilton, C.R. & Vermiere, B.A. (1988). Complementary hemispheric specialisation in monkeys. Science, 242, 1691-1693.
36. Haxby, J.V., Grady, C.L., Horwitz, B., Ungerleider, L.G., Miskin, M., Carson, R.E., Herscovich, P., Schapiro, M.B. & Rapoport, S.I. (1991). Dissociation of spatial and object visual processing pathways in the human extra striate cortex. Proc. Natl Acad. Sci. USA, 88, 1621-1625.
37. Haxby, J.V., Horwitz, B., Ungerleider, L.G., Maisog, J.M., Pietrini, P. & Grady, C.L. (1994). The functional organisation of human extrastriate cortex. A PET rCRF study of selective attention to faces and location. J. Neurosci., 14, 6336-6353.
38. Haxby, J.V., Ungerleider, L.G., Horwitz, B., Maisog, J.M., Rapoport, S.I. & Grady, C.L. (1996). Face encoding and recognition in the human brain. Proc. Natl Acad. Sci. USA, 93, 922-927.
39. Hietanen, J.K., Perrett, D.J., Oram, M.W., Benson, P.J. & Dittrich, W.H. (1991). The effects of lighting conditions on responses of cells selective for face views in the macaque temporal cortex. Exp. Brain Res., 89, 157-171.
40. Hilliard, R.D. (1973). Hemispheric laterally effects on facial recognition tasks in normal subjects. Cortex, 9, 246-258.
41. Kanwisher, N., Chun, M.M., McDermott, J. & Ledden, P.J. (1996). Functional imaging of human visual recognition. Cognit. Brain Res., 5, 55-67.
42. Kanwisher, N., Tong, F. & Nakayama, K. (1998). The effect of face inversion on the human fusiform face area. Cognition, 68, 1-11.
43. Kendrick, K.M. & Baldwin, B.A. (1987). Cells in the temporal cortex of the sheep can respond preferentially to the sight of faces. Science, 236, 448-450.
44. Kendrick, K.M. & Baldwin, B.A. (1989). Visual responses of sheep temporal cortex to moving and stationary human images. Neurosci. Lett., 100, 193-197.
45. Kendrick, K.M. (1990). Neural processing of visual recognition of individuals in sheep. In Zayan, R. & Danzer, D. (eds), Social Stress in Domestic Animals. Kluwer Academic Publications, Dordrecht, The Netherlands, pp. 145-156.
46. Kendrick, K.M. & Baldwin, B.A. (1991). Single unit recording in conscious sheep. Methods Neurosci., 4, 3-15.
47. Kendrick, K.M. (1991). How the sheep brain controls the visual recognition of animals and humans. J. Anim. Sci., 69, 5008-5016.
48. Kendrick, K.M. (1994). Neurobiological correlates of visual and olfactory recognition in sheep. Behav. Proc., 33, 89-112.
49. Kendrick, K.M., Atkins, K.L., Hinton, M.R., Broad, K.D., Fabre-Nys, C. & Keverne, E.B. (1995). Facial and vocal discrimination in sheep. Animal Behav., 49, 1665-1676.
50. Kendrick, K.M., Atkins, K.L., Hinton, M.R., Heavens, P. & Keverne, B, (1996). Are faces special for sheep? Evidence from facial and object discrimination learning tests showing effects of inversion and social familiarity. Behav. Proc., 38, 19-35.
51. Kendrick, K.M., Mimmack, M.L., da Costa, A.P.C. & Broad, K.D. (1998). c-fos mapping of neural substrates involved in face recognition in sheep. Soc. Neurosci. Abstr., 24, 355.10.
52. Leonard, C.M., Rolls, E.T., Wilson, F.A.W. & Bayliss, G.C. (1985). Neurons in the amygdala of the monkey with responses selective for faces. Behav. Brain Res., 15, 159-176.
53. Marston, H.M., West, H.L., Wilkinson, L.S., Everitt, B.J. & Robbins, T.W. (1994). Effects of excitotoxic lesions of the septum and vertical limb nucleus of the diagonal band of Broca on conditional visual discrimination: relationship between performance and choline acetyltransferase activity in the cingulate cortex. J. Neurosci., 14, 2009-2019.
54. McCabe, B.J. & Horn, G. (1994). Learning related changes in Fos-like immunoreactivity in the chick forebrain after imprinting. Proc. Natl Acad. Sci. USA., 91, 11417-11421.
55. McGeorge, A.J. & Faull, R.L.M. (1989). The organisation of the projection from the cerebral cortex to the striatum in the rat. Neuroscience., 29, 503-537.
56. Milner, A.D. & Dunne, J.J. (1977). Lateralised perception of bilateral chimeric faces by normal subjects. Nature., 268, 175-176.
57. Morgan, J.I. & Curran, T. (1991). Stimulus transcription coupling in the nervous system: involvement of the inducable prolo-oncogenes fos and jun. Annu. Rev. Neurosci., 14, 421-451.
58. Morris, R.D. & Hopkins, W.D. (1993). Perception of human chimeric faces by chimpanzees: evidence for a right hemisphere advantage. Brain. Cognit., 21, 11-122.
59. Muir, J.L., Dunnett, S.B., Robbins, T.W. & Everitt, B.J. (1992). Attentional function of the forebrain cholinergic system: effects of intraventricular hemicholium, basal forebrain lesions and intracortical grafts of a multiple choice serial reaction time task. Exp. Brain Res., 89, 611-622.
60. Musil, S.Y. & Olson, C.R. (1993). The role of the cat cingulate cortex in sensoriomotor integration. In Vogt, B.A. & Gabriel, M. (eds), Neurobiology of Cingulate Cortex and the Limbic Thalamus: a Comprehensive Handbook. Birkhäuser, Boston, pp. 345-365.
61. Nicol, A.U., Brown, M.W. & Horn, G. (1995). Neurophysiological investigations of a recognition memory system for imprinting in the domestic chick. Eur. J. Neurosci., 7, 766-776.
62. Ohkura, S., Fabre-Nys, C., Broad, K.D. & Kendrick, K.M. (1997). Sex hormones enhance the impact of male sensory cues on both primary and association cortical components of visual and olfactory processing pathways as well as in limbic and hypothalamic regions in female sheep. Neuroscience, 80, 285-297.
63. Overman, W.A. & Doty, R.W. (1982). Hemispheric specialisation by man but not macaques for analysis of faces. Neuropsychologica, 20, 113-128.
64. Paus, T., Petrides, M., Evans, A.C. & Mayer, E. (1993). Role of the anterior cingulate cortex in the control of oculomotor, manual and speech responses: a positron emission tomography study. J. Neurophysiol., 70, 453-169.
65. 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.
66. Perrett, D.I., Smith, P.A.J., Potter, D.D., Mistlin, A.J., Head, A.S., Milner, A.D. & Jeeves, M.A. (1984) Neurones responsive to faces in the temporal cortex: studies of functional organisation, sensitivity to identity and relation to perception. Hum. Neurobiol., 3, 197-208.
67. Perrett, D.I., Smith, P.A.J., Potter, D.D., Mistlin, A.J., Head, A.S., Milner, A.D. & Jeeves, M.A. (1985). Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc. R. Soc. Lond. B Biol Sci., 223, 293-317.
68. Perrett, D.I., Mistin, A.J. & Chitty, A.J. (1987). Visual neurones responsive to faces. Trends. Neurosci., 10, 358-364.
69. Perrett, D.I., Mistlin, A.J., Chitty, A.J., Smith, P.A., Potter, D.D., Broenniman, R. & Harries, M. (1988). Specialised face processing and hemispheric asymmetry in man and monkey: evidence from single unit and reaction time studies. Behav. Brain Res., 29, 245-258.
70. Peirce, J.W., Leigh, A.E., da Costa, A.P.C. & Kendrick, K.M, (1998). Neural encoding of faces in the sheep. Efffects of asymmetry, configeration and familiarity. Soc. Neurosci. Abstr., 24, 355.9.
71. Peirce, J.W., Leigh, A.E. & Kendrick, K.M. (2000). Configeral coding, familiarity and the right hemisphere advantage for face recognition in sheep. Neuropsychologia, (in press).
72. Puce, A., Allison, T., Gore, J.C. & McCarthy, G. (1995). Face sensitive regions in human extrastriate cortex studied by functional MRI. J. Neurophysiol., 74, 1192-1200.
73. Rosler, A., Lanquillon, S., Dippel, O. & Braune, H.J. (1997). Impairment of facial recognition in patients with right cerebral infarcts quantified by computer-aided 'morphing'. J. Neurol Neurosurg. Psychiatry, 62, 261-264.
74. Scali, C., Casementi, F., Pazzagli, M., Bartolini, L. & Pepeu, G. (1994). Nerve growth factor increases extracellular acetylcholine levels in the parietal cortex and hippocampus of aged rats and restores object recognition. Neurosci. Lett., 170, 117-120.
75. Schwartz, M. & Smith, N. (1980). Visual asymmetries with chimeric faces. Neuropsychologia, 18, 103-106.
76. Seamans, J.K., Floresco, S.B. & Phillips, A.C. (1995). Functional differences between the prelimbic and anterior cingulate regions of the rat pre-frontal cortex. Behav. Neurosci., 109, 1063-1073.
77. Seeck, M., Mainwaring, N., Ives, J., Blume, H., Dubuisson, D., Cosgrove, R., Mesulam, M.M. & Schomer, D.L. (1993). Differential neural activity in the human temporal lobe evoked by faces of family members and friends. Ann. Neurol., 34, 369-372.
78. Seeck, M., Michel, C.M., Mainwaring, N., Cosgrove, R., Blume, H., Ives, J., Landis, T. & Schomer, D.L. (1997). Evidence for rapid face recognition from human scalp and intracranial electrodes. Neuroreport, 8, 2749-2754.
79. Sergent, J. & Bindra, D. (1981) Differential hemispheric processing of faces: methodological considerations and reinterpretation. Psychol. Bull., 89, 541-554.
80. Sergent, J., Ohta, S. & MacDonald, B. (1992). Functional neuroanatomy face and object processing: a positron emission tomography study. Brain, 115, 15-36.
81. Snyder, L.H., Batista, A.P. & Andersen, R.A. (1997). Coding of intention in the posterior parietal cortex. Nature, 386, 167-171.
82. Ungerleider, L.G., Gaffan, D. & Pelak, V.S. (1989). Projections from inferior temporal cortex to prefrontal cortex via the uncinate fasicle in the rhesus monkey. Exp. Brain Res., 76, 473-484.
83. van Hoesen, G.W., Rosene, D.L. & Mesulam, M.M. (1979). Subicular input from the temporal cortex in the rhesus monkey. Science, 205, 608-610.
84. van Strafen, F., Muller, R., Curran, T., van Beveren, C. & Verma, I. (1983). Complete nucleotide sequence of a human c-onc gene: Deduced amino acid sequence of the human c-fos protein. Proc. Natl Acad. Sci. USA, 80, 3183-3187.
85. Vermeire, B.A. & Hamilton, C.R. (1998). Inversion effect for faces in split-brain monkeys. Neurophyschologia, 36, 1003-1014.
86. Vogt, B.A. (1985). Cingulate cortex. In Peters, A. & Jones, E.G. (eds), Cerbral Cortex: Vol. 4. Association and Auditory Cortices. Plenum, New York, pp. 89-149.
87. Vogt, B.A., Finch, D.M. & Olson, C.R. (1992). Functional heterogeneity in cingulate cortex: the anterior executive and posterior evaluative regions. Cereb. Cortex, 2, 435-443.
88. Webster, M.J., Bachevalier, J. & Ungerleider, L.G. (1994). Connections of inferior temporal area TEO and TE with the parietal and frontal cortex in macaque monkeys. Cereb. Cortex, 5, 470-483.
89. Zhu, X.O., McCabe, B.J., Aggleton, J.P. & Brown, M.W. (1997). Differential activation of the rat hippocampus and perirhinal cortex by novel visual stimuli and a novel enviroment. Neurosci. Lett., 29, 141-143.
90. Zhu, X.O., Brown, M.W., McCabe, B.J. & Aggleton, J.P. (1995). Effects of the novelty or familiarity of visual stimulation on the expression of the early gene c-fos in rat brain. Neuroscience, 69, 821-829.