Neural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala

Neuroscience

Volumn 169, Issue 1, 2010, Pages 287-301

  Tazumi, T ^a   Hori, E ^a   Maior, R S ^a   Ono, T ^a   Nishijo, H ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Amygdala; Face neurons; Gaze direction; Head orientation; Monkey; Social cognition

Indexed keywords

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; GAZE; MACACA; NONHUMAN; PRIORITY JOURNAL; SPATIAL DISCRIMINATION; SPATIAL ORIENTATION; STIMULUS RESPONSE;

AMYGDALA; ANIMALS; FACE; FIXATION, OCULAR; HEAD; HUMANS; MACACA; NEURONS; PATCH-CLAMP TECHNIQUES; PATTERN RECOGNITION, VISUAL; PHOTIC STIMULATION; POSTURE; SOCIAL BEHAVIOR; SPECIES SPECIFICITY; STEREOTAXIC TECHNIQUES;

EID: 77953807932     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2010.04.028     Document Type: Article

References (75)

1. Abell F., Krams M., Ashburner J., Passingham R., Friston K., Frackowiak R., Happe F., Frith C., Frith U. The neuroanatomy of autism: a voxel-based whole brain analysis of structural scans. Neuroreport 1999, 10:1647-1651.
2. Adams R.B., Gordon H.L., Baird A.A., Ambady N., Kleck R.E. Effects of gaze on amygdala sensitivity to anger and fear faces. Science 2003, 300:1536.
3. Adolphs R., Gosselin F., Buchanan T.W., Tranel D., Schyns P., Damasio A.R. A mechanism for impaired fear recognition after amygdala damage. Nature 2005, 433:68-72.
4. Aggleton J.P., Burton M.J., Passingham R.E. Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res 1980, 190:347-368.
5. Aggleton J.P., Saunders R.C. The amygdala-what's happened in the last decade. The amygdala. A functional analysis 2000, 1-30. Oxford University Press, Oxford, UK. 2nd ed. J.P. Aggleton (Ed.).
6. Allison T., Puce A., McCarthy G. Social perception from visual cues: role of the STS region. Trends Cogn Sci 2000, 4:267-278.
7. Amaral D.G., Price J.L., Pitkänen A., Carmichael S.T. Anatomical organization of the primate amygdaloid complex. The amygdala: neurobiological aspects of emotion, memory, and mental dysfunction 1992, 1-66. Wiley-Liss, New York. J.P. Aggleton (Ed.).
8. Argyle M., Cook M. Gaze and mutual gaze 1976, Cambridge University Press, Cambridge, UK.
9. Asahi T., Tamura R., Eifuku S., Hayashi N., Endo S., Nishijo H., Ono T. 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 2003, 47:255-260.
10. Asahi T., Uwano T., Eifuku S., Tamura R., Endo S., Ono T., Nishijo H. Neural responses to a delayed-response delayed-reward go/nogo task in the monkey posterior insular cortex. Neuroscience 2006, 143:627-639.
11. Ashwin C., Baron-Cohen S., Wheelwright S., O'Riordan M., Bullmore E.T. Differential activation of the amygdala and the 'social brain' during fearful face-processing in Asperger Syndrome. Neuropsychologia 2007, 45:2-14.
12. Attwood A., Frith U., Hermelin B. The understanding and use of interpersonal gestures by autistic and Down's syndrome children. J Autism Dev Disord 1988, 18:241-257.
13. Baron-Cohen S. Mindblindness: an essay on autism and theory of mind 1995, MIT Press, Cambridge, MA.
14. Baron-Cohen S., Ring H.A., Wheelwright S., Bullmore E.T., Brammer M.J., Simmons A., Williams S.C. Social intelligence in the normal and autistic brain: an fMRI study. Eur J Neurosci 1999, 11:1891-1898.
15. Bauman M., Kemper T. Limbic and cerebellar abnormalities: consistent findings in infantile autism. J Neuropathol Exp Neurol 1988, 47:369.
16. Bieber S.L., Smith D.V. Multivariate analysis of sensory data: a comparison of methods. Chem Senses 1986, 11:19-47.
17. Brothers L., Ring B. Mesial temporal neurons in the macaque monkey with responses selective for aspects of social stimuli. Behav Brain Res 1993, 57:53-61.
18. Carmel D., Bentin S. Domain specificity versus expertise: factors influencing distinct processing of faces. Cognition 2002, 83:1-29.
19. Corden B., Critchley H.D., Skuse D., Dolan R.J. Fear recognition ability predicts differences in social cognitive and neural functioning in men. J Cogn Neurosci 2006, 18:889-897.
20. Dalton K.M., Nacewicz B.M., Johnstone T., Schaefer H.S., Gernsbacher M.A., Goldsmith H.H., Alexander A.L., Davidson R.J. Gaze fixation and the neural circuitry of face processing in autism. Nat Neurosci 2005, 8:519-526.
21. Demos K.E., Kelley W.M., Ryan S.L., Davis F.C., Whalen P.J. Human amygdala sensitivity to the pupil size of others. Cereb Cortex 2008, 18:2729-2734.
22. De Souza W.C., Eifuku S., Tamura R., Nishijo H., Ono T. Differential characteristics of face neuron responses within the anterior superior temporal sulcus of macaques. J Neurophysiol 2005, 94:1252-1266.
23. Dziobek I., Fleck S., Rogers K., Wolf O.T., Convit A. The 'amygdala theory of autism' revisited: linking structure to behavior. Neuropsychologia 2006, 44:1891-1899.
24. Eifuku S., De Souza W.C., Tamura R., Nishijo H., Ono T. Neuronal correlates of face identification in the monkey anterior temporal cortical areas. J Neurophysiol 2004, 91:358-371.
25. Emery N.J. The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 2000, 24:581-604.
26. Engell A.D., Haxby J.V., Todorov A. Implicit trustworthiness decisions: automatic coding of face properties in the human amygdala. J Cogn Neurosci 2007, 19:1508-1519.
27. Ferrari P.F., Paukner A., Ionica C., Suomi S.J. Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 2009, 19:1768-1772.
28. Frith C.D., Frith U. Interacting minds-a biological basis. Science 1999, 286:1692-1695.
29. Garrett A.S., Menon V., MacKenzie K., Reiss A.L. Here's looking at you, kid: neural systems underlying face and gaze processing in fragile X syndrome. Arch Gen Psychiatry 2004, 61:281-288.
30. George N., Driver J., Dolan R.J. Seen gaze-direction modulates fusiform activity and its coupling with other brain areas during face processing. Neuroimage 2001, 13:1102-1112.
31. Gothard K.M., Battaglia F.P., Erickson C.A., Spitler K.M., Amaral D.G. Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 2007, 97:1671-1683.
32. Guo K., Robertson R.G., Mahmoodi S., Tadmor Y., Young M.P. How do monkeys view faces?-A study of eye movements. Exp Brain Res 2003, 150:363-374.
33. Gómez J.C. Understanding other subjects. Apes, monkeys, children, and the growth of mind 2004, 204-237. Harvard University Press, New York, NY.
34. Hietanen J.K. Does your gaze direction and head orientation shift my visual attention?. Neuroreport 1999, 10:3443-3447.
35. Hoffman K.L., Gothard K.M., Schmid M.C., Logothetis N.K. Facial-expression and gaze-selective responses in the monkey amygdala. Curr Biol 2007, 17:766-772.
36. Hooker C.I., Paller K.A., Gitelman D.R., Parrish T.B., Mesulam M.M., Reber P.J. Brain networks for analyzing eye gaze. Brain Res Cogn Brain Res 2003, 17:406-418.
37. Hori E., Tazumi T., Umeno K., Kamachi M., Kobayashi T., Ono T., Nishijo H. Effects of facial expression on shared attention mechanisms. Physiol Behav 2005, 84:397-405.
38. Howard M.A., Cowell P.E., Boucher J., Broks P., Mayes A., Farrant A., Roberts N. Convergent neuroanatomical and behavioural evidence of an amygdala hypothesis of autism. Neuroreport 2000, 11:2931-2935.
39. Jellema T., Perrett D.I. Neural basis for the perception of goal-directed actions. The cognitive neuroscience of social behavior 2005, 81-112. Psychology Press, New York. A. Easton, N. Emery (Eds.).
40. Johnson M.H. Subcortical face processing. Nat Rev Neurosci 2005, 6:766-774.
41. Johnston J.B. Further contributions to the study of the evolution of the forebrain. J Comp Neurol 1923, 35:337-481.
42. Kawashima R., Sugiura M., Kato T., Nakamura A., Hatano K., Ito K., Fukuda H., Kojima S., Nakamura K. The human amygdala plays an important role in gaze monitoring: a PET study. Brain 1999, 122:779-783.
43. Kobayashi H., Kohshima S. Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye. J Hum Evol 2001, 40:419-435.
44. Kobayashi R., Murata T. Behavioral characteristics of 187 young adults with autism. Psychiatry Clin Neurosci 1998, 52:383-390.
45. Kuraoka K., Nakamura K. Impacts of facial identity and type of emotion on responses of amygdala neurons. Neuroreport 2006, 17:9-12.
46. Kusama T., Mabuchi M. Stereotaxic atlas of the brain of Macaca fuscata 1970, University of Tokyo Press, Tokyo.
47. Langton S.R. The mutual influence of gaze and head orientation in the analysis of social attention direction. Q J Exp Psychol A 2000, 53:825-845.
48. Langton S.R., Honeyman H., Tessler E. The influence of head contour and nose angle on the perception of eye-gaze direction. Percept Psychophys 2004, 66:752-771.
49. Leekam S.R., Ramsden C.A.H. Dyadic orientation and joint attention in preschool children with autism. J Autism Dev Disord 2006, 36:185-197.
50. Leonard C.M., Rolls E.T., Wilson F.A., Baylis G.C. Neurons in the amygdala of the monkey with responses selective for faces. Behav Brain Res 1985, 15:159-176.
51. Matsuda K. Measurement system of the eye positions by using oval fitting of a pupil. Neurosci Res Suppl 1996, 25:270.
52. Nahm F.K.D., Perret A., Amaral D.G., Albright T.D. How do monkeys look at faces?. J Cogn Neurosci 1997, 9:611-623.
53. Nakamura K., Mikami A., Kubota K. Activity of single neurons in the monkey amygdala during performance of a visual discrimination task. J Neurophysiol 1992, 67:1447-1463.
54. Nishijo H., Ono T., Nishino H. Single neuron responses in amygdala of alert monkey during complex sensory stimulation with affective significance. J Neurosci 1988, 8:3570-3583.
55. Nishijo H., Ono T., Nishino H. Topographic distribution of modality-specific amygdalar neurons in alert monkey. J Neurosci 1988, 8:3556-3569.
56. Nishijo H., Ono T., Tamura R., Nakamura K. Amygdalar and hippocampal neuron responses related to recognition and memory in monkey. Prog Brain Res 1993, 95:339-357.
57. Okada T., Sato W., Kubota Y., Usui K., Inoue Y., Murai T., Hayashi T., Toichi M. Involvement of medial temporal structures in reflexive attentional shift by gaze. Soc Cogn Affect Neurosci 2008, 3:80-88.
58. Pageler N.M., Menon V., Merin N.M., Eliez S., Brown W.E., Reiss A.L. Effect of head orientation on gaze processing in fusiform gyrus and superior temporal sulcus. Neuroimage 2003, 20:318-329.
59. Parr L.A., Winslow J.T., Hopkins W.D. Is the inversion effect in rhesus mokeys face-specific?. Anim Cogn 1999, 2:123-129.
60. Pelphrey K.A., Morris J.P., McCarthy G. Neural basis of eye gaze processing deficits in autism. Brain 2005, 128:1038-1048.
61. Perrett D.I., Hietanen J.K., Oram M.W., Benson P.J. Organization and functions of cells responsive to faces in the temporal cortex. Philos Trans R Soc Lond B Biol Sci 1992, 335:23-30.
62. Perrett D.I., Mistlin A.J. Perception of facial characteristics by monkeys. Comparative perception 1990, 187-215. John Wiley, New York. W.C. Stebbins, M.A. Berkley (Eds.).
63. Perrett D.I., Smith P.A., Potter D.D., Mistlin A.J., Head A.S., Milner A.D., Jeeves M.A. Visual cells in the temporal cortex sensitive to face view and gaze direction. Proc R Soc Lond B Biol Sci 1985, 223:293-317.
64. Preuschoft S. "Laughter" and "smile" in Barbary macaques (Macaca sylvanus). Ethology 1992, 91:220-236.
65. Rolls E.T. Functions of the primate temporal lobe cortical visual areas in invariant visual object and face recognition. Neuron 2000, 27:205-218.
66. Rolls E.T., Judge S.J., Sanghera M.K. Activity of neurons in the inferotemporal cortex of the alert monkey. Brain Res 1977, 130:229-238.
67. Sato N., Nakamura K. Detection of directed gaze in rhesus monkeys (Macaca mulatta). J Comp Psychol 2001, 115:115-121.
68. Schumann C.M., Amaral D.G. Stereological analysis of amygdala neuron number in autism. J Neurosci 2006, 26:7674-7679.
69. Spezio M.L., Huang P.Y., Castelli F., Adolphs R. Amygdala damage impairs eye contact during conversations with real people. J Neurosci 2007, 27:3994. 3397.
70. Todorovic D. Geometrical basis of perception of gaze direction. Vision Res 2006, 46:3549-3562.
71. Tomasello M., Hare B., Lehmann H., Call J. Reliance on head versus eyes in the gaze following of great apes and human infants: the cooperative eye hypothesis. J Hum Evol 2007, 52:314-320.
72. Turner B.H., Mishkin M., Knapp M. Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J Comp Neurol 1980, 191:515-543.
73. Welchew D.E., Ashwin C., Berkouk K., Salvador R., Suckling J., Baron-Cohen S., Bullmore E. Functional disconnectivity of the medial temporal lobe in Asperger's syndrome. Biol Psychiatry 2005, 57:991-998.
74. Wilson H.R., Wilkinson F., Lin L.M., Castillo M. Perception of head orientation. Vision Res 2000, 40:459-472.
75. Young A.W., Aggleton J.P., Hellawell D.J., Johnson M., Broks P., Hanley J.R. Face processing impairments after amygdalotomy. Brain 1995, 118:15-24.