Neurons responsive to face-view in the primate ventrolateral prefrontal cortex

Neuroscience

Volumn 189, Issue , 2011, Pages 223-235

  Romanski, L M ^a   Diehl, M M ^a  

^a UNIVERSITY OF ROCHESTER   (United States)

Author keywords

Communication; Face cells; Gaze; Multisensory integration; Prefrontal cortex; Vocalizations

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; BRAIN NERVE CELL; CONTROLLED STUDY; FACE; GAZE; HUMAN; INTERPERSONAL COMMUNICATION; LANGUAGE; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RHESUS MONKEY; STIMULUS RESPONSE; VENTROLATERAL PREFRONTAL CORTEX; VISUAL STIMULATION; VOCALIZATION;

ACOUSTIC STIMULATION; ANIMALS; FACE; FACIAL EXPRESSION; HUMANS; MACACA MULATTA; MOTION PERCEPTION; NEURONS; PHOTIC STIMULATION; PREFRONTAL CORTEX; PSYCHOMOTOR PERFORMANCE; VOCALIZATION, ANIMAL;

EID: 79960911516     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.05.014     Document Type: Article

References (79)

1. Averbeck B.B., Crowe D.A., Chafee M.V., Georgopoulos A.P. Neural activity in prefrontal cortex during copying geometrical shapes. II. Decoding shape segments from neural ensembles. Exp Brain Res 2003, 150:142-153.
2. Barbas H. Flow of information for emotions through temporal and orbitofrontal pathways. J Anat 2007, 211(2):237-249.
3. Barbas H. Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res Bull 2000, 52(5):319-330.
4. Barbas H. Architecture and cortical connections of the prefrontal cortex in the rhesus monkey. Adv Neurol 1992, 57:91-115. [Review].
5. Borst A., Theunissen F.E. Information theory and neural coding. Nat Neurosci 1999, 2:947-957.
6. Breiter H.C., Etcoff N.L., Whalen P.J., Kennedy W.A., Rauch S.L., Buckner R.L., Strauss M.M., Hyman S.E., Rosen B.R. Response and habituation of the human amygdala during visual processing of facial expression. Neuron 1996, 17(5):875-887.
7. Carmichael S.T., Price J.L. Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. J Comp Neurol 1995, 363:615-641.
8. Davis M., Whalen P.J. The amygdala: vigilance and emotion. Mol Psychiatry 2001, 6(1):13-34.
9. Diehl M.M., Bartlow-Kang J., Sugihara T., Romanski L.M. Distinct temporal lobe projections to auditory and visual regions in the ventral prefrontal cortex support face and vocalization processing 2008, Program No. 387.25. 2008 Neuroscience Meeting Planner, Society for Neuroscience, Washington, DC, Online.
10. Dolan R.J., Fletcher P., Morris J., Kapur N., Deakin J.F., Frith C.D. Neural activation during covert processing of positive emotional facial expressions. Neuroimage 1996, 4(3 Pt 1):194-200.
11. 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.
12. Engell A.D., Haxby J.V. Facial expression and gaze-direction in human superior temporal sulcus. Neuropsychologia 2007, 45(14):3234-3241.
13. Freiwald W.A., Tsao D.Y. Functional compartmentalization and viewpoint generalization within the macaque face-processing system. Science 2010, 330(6005):845-851.
14. Ghazanfar A.A., Nielsen K., Logothetis N.K. Eye movements of monkey observers viewing vocalizing conspecifics. Cognition 2006, 101(3):515-529.
15. Golomb D., Hertz J., Panzeri S., Treves A., Richmond B. How well can we estimate the information carried in neuronal responses from limited samples?. Neural Comput 1997, 9:649-665.
16. 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(2):1671-1683.
17. Gothard K.M., Brooks K.N., Peterson M.A. Multiple perceptual strategies used by macaque monkeys for face recognition. Anim Cogn 2009, 12(1):155-167.
18. Haith M.M., Bergman T., Moore M.J. Eye contact and face scanning in early infancy. Science 1977, 198(4319):853-855.
19. Hasselmo M.E., Rolls E.T., Baylis G.C. The role of expression and identity in the face-selective responses of neurons in the temporal visual cortex of the monkey. Behav Brain Res 1989, 32:203-218.
20. Haxby J.V., Hoffman E.A., Gobbini M.I. Human neural systems for face recognition and social communication. Biol Psychiatry 2002, 51(1):59-67.
21. 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(9):766-772.
22. Iidaka T., Omori M., Murata T., Kosaka H., Yonekura Y., Okada T., Sadato N. Neural interaction of the amygdala with the prefrontal and temporal cortices in the processing of facial expressions as revealed by fMRI. J Cogn Neurosci 2001, 13(8):1035-1047.
23. Ishai A., Pessoa L., Bikle P.C., Ungerleider L.G. Repetition suppression of faces is modulated by emotion. Proc Natl Acad Sci U S A 2004, 101(26):9827-9832.
24. Ishai A., Schmidt C.F., Boesiger P. Face perception is mediated by a distributed cortical network. Brain Res Bull 2005, 67(1-2):87-93.
25. Johnson R.A., Wichern D.W. Applied multivariate statistical analysis 1998, Prentice Hall, Saddle River, NJ.
26. Kalin N.H., Shelton S.E. Defensive behaviors in infant rhesus monkeys: environmental cues and neurochemical regulation. Science 1989, 243(4899):1718-1721.
27. Kanwisher N., McDermott J., Chun M.M. The fusiform face area: a module in human extrastriate cortex specialized for face perception. J Neurosci 1997, 17(11):4302-4311.
28. 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(Pt 4):779-783.
29. Kesler-West M.L., Andersen A.H., Smith C.D., Avison M.J., Davis C.E., Kryscio R.J., Blonder L.X. Neural substrates of facial emotion processing using fMRI. Brain Res Cogn Brain Res 2001, 11(2):213-226.
30. Klin A., Jones W., Schultz R., Volkmar F., Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Arch Gen Psychiatry 2002, 59(9):809-816.
31. Kowatari Y., Yamamoto M., Takahashi T., Kansaku K., Kitazawa S., Ueno S., Yamane S. Dominance of the left oblique view in activating the cortical network for face recognition. Neurosci Res 2004, 50(4):475-480.
32. Kuraoka K., Nakamura K. Responses of single neurons in monkey amygdala to facial and vocal emotions. J Neurophysiol 2007, 97(2):1379-1387.
33. LeDoux J. The amygdala. Curr Biol 2007, 17(20):R868-R874.
34. 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(2):159-176.
35. Liu C.H., Chaudhuri A. Reassessing the 3/4 view effect in face recognition. Cognition 2002, 83(1):31-48.
36. Logie R.H., Baddeley A.D., Woodhead M.M. Face recognition, pose and ecological validity. Appl Cogn Psychol 1987, 1:53-69.
37. LoPresti M.L., Schon K., Tricarico M.D., Swisher J.D., Celone K.A., Stern C.E. Working memory for social cues recruits orbitofrontal cortex and amygdala: a functional magnetic resonance imaging study of delayed matching to sample for emotional expressions. J Neurosci 2008, 28(14):3718-3728.
38. Morris J.S., Frith C.D., Perrett D.I., Rowland D., Young A.W., Calder A.J., Dolan R.J. A differential neural response in the human amygdala to fearful and happy facial expressions. Nature 1996, 383(6603):812-815.
39. Nahm F.K., Perret A., Amaral D.G., Albright T.D. How do mokeys look at faces?. J Cogn Neurosci 1997, 9(5):611.
40. Nomura M., Ohira H., Haneda K., Iidaka T., Sadato N., Okada T., Yonekura Y. Functional association of the amygdala and ventral prefrontal cortex during cognitive evaluation of facial expressions primed by masked angry faces: an event-related fMRI study. Neuroimage 2004, 21(1):352-363.
41. Optican L.M., Gawne T.J., Richmond B.J., Joseph P.J. Unbiased measures of transmitted information and channel capacity from multivariate neuronal data. Biol Cybern 1991, 65:305-310.
42. O'Scalaidhe S.P., Goldman-Rakic P.S. Memory fields in the prefrontal cortex of the macaque. Soc Neurosci Abstr 1993, 19(326):6.
43. O'Scalaidhe S.P., Wilson F.A., Goldman-Rakic P.S. Areal segregation of face-processing neurons in prefrontal cortex. Science 1997, 278:1135-1138.
44. O'Scalaidhe S.P.O., Wilson F.A.W., Goldman-Rakic P.G.R. Face-selective neurons during passive viewing and working memory performance of rhesus monkeys: evidence for intrinsic specialization of neuronal coding. Cereb Cortex 1999, 9:459-475.
45. Panzeri S., Senatore R., Montemurro M.A., Petersen R.S. Correcting for the sampling bias problem in spike train information measures. J Neurophysiol 2007, 98(3):1064-1072.
46. Panzeri S., Treves A. Analytical estimates of limited sampling biases in different information measures. Network 1996, 7:87-107.
47. Parr L.A., Winslow J.T., Hopkins W.D. Is the inversion effect in rhesus monkeys face specific?. Anim Cogn 1999, 2:123-129.
48. 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(1232):293-317.
49. Petrides M., Pandya D.N. Comparative cytoarchitectonic analysis of the human and the macaque ventrolateral prefrontal cortex and corticocortical connection patterns in the monkey. Eur J Neurosci 2002, 16(2):291-310.
50. Pourtois G., Schwartz S., Seghier M.L., Lazeyras F., Vuilleumier P. Neural systems for orienting attention to the location of threat signals: an event-related fMRI study. Neuroimage 2006, 31(2):920-933.
51. Preuss T.M., Goldman-Rakic P.S. Myelo- and cytoarchitecture of the granular frontal cortex and surrounding regions in the strepsirhine primate Galago and the anthropoid primate Macaca. J Comp Neurol 1991, 310:429-474.
52. Rolls E.T. The orbitofrontal cortex. Philos Trans R Soc Lond B Biol Sci 1996, 351(1346):1433-1443. discussion: 1443-1444.
53. Rolls E.T., Treves A., Tovee M.J. The representational capacity of the distributed encoding of information provided by populations of neurons in primate temporal visual cortex. Exp Brain Res 1997, 114:149-162.
54. Romanski L.M., Averbeck B.B., Diltz M. Neural representation of vocalizations in the primate ventrolateral prefrontal cortex. J Neurophysiol 2005, 93(2):734-747.
55. Romanski L.M., Bates J.F., Goldman-Rakic P.S. Auditory belt and parabelt projections to the prefrontal cortex in the rhesus monkey. J Comp Neurol 1999, 403:141-157.
56. Romanski L.M., Goldman-Rakic P.S. An auditory domain in primate prefrontal cortex. Nat Neurosci 2002, 5:15-16.
57. Romanski L.M., Tian B., Fritz J., Mishkin M., Goldman-Rakic P.S., Rauschecker J.P. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nat Neurosci 1999, 2(12):1131-1136.
58. Sakaguchi Y., Ishida F., Shimizu T., Murata A. Time course of information representation of macaque AIP neurons in hand manipulation task revealed by information analysis. J Neurophysiol 2010, 104(6):3625-3643.
59. Saleem K.S., Kondo H., Price J.L. Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey. J Comp Neurol 2008, 506(4):659-693.
60. Sergerie K., Lepage M., Armony J.L. A face to remember: emotional expression modulates prefrontal activity during memory formation. Neuroimage 2005, 24(2):580-585.
61. Stephan B.C., Caine D. What is in a view?. The role of featural information in the recognition of unfamiliar faces across viewpoint transformation. Perception 2007, 36(2):189-198.
62. Sugase Y., Yamane S., Ueno S., Kawano K. Global and fine information coded by single neurons in the temporal visual cortex. Nature 1999, 400(6747):869-873.
63. Sugihara T., Diltz M.D., Averbeck B.B., Romanski L.M. Integration of auditory and visual communication information in the primate ventrolateral prefrontal cortex. J Neurosci 2006, 26:11138-11147.
64. Suzuki H., Azuma M. Topographic studies on visual neurons in the dorsolateral prefrontal cortex of the monkey. Exp Brain Res 1983, 53:47-58.
65. Tazumi T., Hori E., Maior R.S., Ono T., Nishijo H. Neural correlates to seen gaze-direction and head orientation in the macaque monkey amygdala. Neuroscience 2010, 169(1):287-301.
66. Thorpe S.J., Rolls E.T., Maddison S. The orbitofrontal cortex: neuronal activity in the behaving monkey. Exp Brain Res 1983, 49:93-115.
67. Treves A., Panzeri S. The upward bias in measures of information derived from limited data samples. Neural Comput 1995, 7:399-407.
68. Tsao D.Y., Freiwald W.A., Knutsen T.A., Mandeville J.B., Tootell R.B. Faces and objects in macaque cerebral cortex. Nat Neurosci 2003, 6:989-995.
69. Tsao D.Y., Freiwald W.A., Tootell R.B., Livingstone M.S. A cortical region consisting entirely of face-selective cells. Science 2006, 311:670-674.
70. Tsao D.Y., Schweers N., Moeller S., Freiwald W.A. Patches of face-selective cortex in the macaque frontal lobe. Nat Neurosci 2008, 11(8):877-879.
71. Van der Linde I., Watson T. A combinatorial study of pose effects in unfamiliar face recognition. Vis Res 2010, 50(5):522-533.
72. Victor J.D., Purpura K.P. Nature and precision of temporal coding in visual cortex: a metric-space analysis. J Neurophysiol 1996, 76(2):1310-1326.
73. Vinette C., Gosselin F., Schyns P.G. Spatio-temporal dynamics of face recognition in a flash: it's in the eyes. Cogn Sci 2004, 28:289-301.
74. Vuilleumier P., Armony J.L., Driver J., Dolan R.J. Effects of attention and emotion on face processing in the human brain. An event-related fMRI study. Neuron 2001, 30(3):829-841.
75. Webster M.J., Bachevalier J., Ungerleider L.G. Connections of inferior temporal areas TEO and TE with parietal and frontal cortex in macaque monkeys. Cereb Cortex 1994, 4:470-483.
76. Wilson F.A., Goldman-Rakic P.S. Viewing preferences of rhesus monkeys related to memory for complex pictures, colours and faces. Behav Brain Res 1994, 60(1):79-89.
77. Wilson F.A., O'Scalaidhe S.P., Goldman-Rakic P.S. Dissociation of object and spatial processing domains in primate prefrontal cortex. Science 1993, 260:1955-1958.
78. Wirth S., Avsar E., Chiu C.C., Sharma V., Smith A.C., Brown E., Suzuki W.A. Trial outcome and associative learning signals in the monkey hippocampus. Neuron 2009, 61(6):930-940.
79. Young M.P., Yamane S. Sparse population coding of faces in the inferotemporal cortex. Science 1992, 256:1327-1331.