The role of superior temporal sulcus in the control of irrelevant emotional face processing: A transcranial direct current stimulation study

Neuropsychologia

Volumn 64, Issue , 2014, Pages 124-133

  Tseng, Lin Yuan ^a,b   Tseng, Philip ^a,c   Liang, Wei Kuang ^a   Hung, Daisy L ^a,b   Tzeng, Ovid J L ^a,b,d   Muggleton, Neil G ^a,e   Juan, Chi Hung ^a  

^a NATIONAL CENTRAL UNIVERSITY   (Taiwan)

^b NATIONAL YANG MING UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

^d INSTITUTE OF LINGUISTICS   (Taiwan)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Emotion; Facial expressions; Frontal eye field; Saccade curvatures; Saccade latency; Superior temporal sulcus; TDCS

Indexed keywords

ADULT; ARTICLE; BRAIN FUNCTION; EMOTION; EYE MOVEMENT; FACIAL EXPRESSION; FEAR; FEMALE; FRONTAL EYE FIELD; HUMAN; HUMAN EXPERIMENT; MALE; NEUROMODULATION; NORMAL HUMAN; SACCADIC EYE MOVEMENT; SELECTIVE ATTENTION; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; TRANSCRANIAL DIRECT CURRENT STIMULATION; VISUAL DISCRIMINATION; ATTENTION; FACIAL RECOGNITION; PHOTOSTIMULATION; PHYSIOLOGY; TEMPORAL LOBE; VISUAL FIELD; YOUNG ADULT;

ADULT; ATTENTION; EMOTIONS; FACIAL EXPRESSION; FACIAL RECOGNITION; FEMALE; HUMANS; MALE; PHOTIC STIMULATION; SACCADES; TEMPORAL LOBE; TRANSCRANIAL DIRECT CURRENT STIMULATION; VISUAL FIELDS; YOUNG ADULT;

EID: 84922428800     PISSN: 00283932     EISSN: 18733514     Source Type: Journal    
DOI: 10.1016/j.neuropsychologia.2014.09.015     Document Type: Article

References (97)

1. Amaral D.G., Behniea H., Kelly J.L. Topographic organization of projections from the amygdala to the visual cortex in the macaque monkey. Neuroscience 2003, 118:1099-1120.
2. Antal A., Kovács G., Chaieb L., Cziraki C., Paulus W., Greenlee M.W. Cathodal stimulation of human MT+ leads to elevated fMRI signal: a tDCS-fMRI study. Restor. Neurol. Neurosci. 2012, 30(3):255-263.
3. Antal A., Polania R., Schmidt-Samoa C., Dechent P., Paulus W. Transcranial direct current stimulation over the primary motor cortex during fMRI. NeuroImage 2011, 55(2):590-596.
4. Bannerman R.L., Milders M., de Gelder B., Sahraie A. Orienting to threat: faster localization of fearful facial expressions and body postures revealed by saccadic eye movements. Proc. Biol. Sci. 2009, 276:1635-1641.
5. Bannerman R.L., Milders M., Sahraie A. Processing emotional stimuli: comparison of saccadic and manual choice-reaction times. Cogn. Emot. 2009, 23:930-954.
6. Bannerman R.L., Milders M., Sahraie A. Attentional bias to brief threat-related faces revealed by saccadic eye movements. Emotion 2010, 10:733-738.
7. Bichot N.P., Schall J.D. Priming in macaque frontal cortex during popout visual search: feature-based facilitation and location-based inhibition of return. J. Neurosci. 2002, 22:4675-4685.
8. Bikson M., Datta A. Guidelines for precise and accurate computational models of tDCS. Brain stimulation 2012, 5(3):430.
9. Bindman L.J., Lippold O.C., Redfearn J.W. The action of brief polarizing currents on the cereb cortex of the rat (1) during current flow and (2) in the production of long-lasting after-effects. J. Physiol. 1964, 172:369-382.
10. Bressler S.L., Tang W., Sylvester C.M., Shulman G.L., Corbetta M. Top-down control of human visual cortex by frontal and parietal cortex in anticipatory visual spatial attention. J. Neurosci. 2008, 28:10056-10061.
11. Britton J.C., Taylor S.F., Sudheimer K.D., Liberzon I. Facial expressions and complex IAPS pictures: common and differential networks. NeuroImage 2006, 31:906-919.
12. Bruce V., Young A. Understanding face recognition. Br. J. Psychol. 1986, 77(Pt 3):305-327.
13. Candidi M., Stienen B.M., Aglioti S.M., de Gelder B. Event-related repetitive transcranial magnetic stimulation of posterior superior temporal sulcus improves the detection of threatening postural changes in human bodies. J. Neurosci. 2011, 31:17547-17554.
14. Chambers C.D., Heinen K. TMS and the functional neuroanatomy of attention. Cortex 2010, 46:114-117.
15. Chambers C.D., Payne J.M., Stokes M.G., Mattingley J.B. Fast and slow parietal pathways mediate spatial attention. Nat. Neurosci. 2004, 7:217-218.
16. Chang C.F., Hsu T.Y., Tseng P., Liang W.K., Tzeng O.J., Hung D.L., Juan C.H. Right temporoparietal junction and attentional reorienting. Hum. Brain Mapp. 2013, 34(4):869-877.
17. Chao C.M., Tseng P., Hsu T.Y., Su J.H., Tzeng O.J., Hung D.L., Muggleton N.G., Juan C.H. Predictability of saccadic behaviors is modified by transcranial magnetic stimulation over human posterior parietal cortex. Hum. Brain Mapp. 2011, 32:1961-1972.
18. Chen L.-F., Yen Y.-S. Taiwanese Facial Expression Image Database 2007, Brain Mapping Laboratory, Institute of Brain Science, National Yang-Ming University, Taipei, Taiwan.
19. Chen-Harris H., Joiner W.M., Ethier V., Zee D.S., Shadmehr R. Adaptive control of saccades via internal feedback. J. Neurosci. 2008, 28:2804-2813.
20. Corbetta M., Shulman G.L. Control of goal-directed and stimulus-driven attention in the brain. Nat. Rev. Neurosci. 2002, 3:201-215.
21. Creutzfeldt O.D., Fromm G.H., Kapp H. Influence of transcortical d-c currents on cortical neuronal activity. Exp. Neurol. 1962, 5:436-452.
22. Dayan E., Censor N., Buch E.R., Sandrini M., Cohen L.G. Noninvasive brain stimulation: from physiology to network dynamics and back. Nat. Neurosci. 2013, 16(7):838-844.
23. de Gelder B., Partan S. The neural basis of perceiving emotional bodily expressions in monkeys. NeuroReport 2009, 20:642-646.
24. Desimone R., Duncan J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 1995, 18:193-222.
25. Dolan R.J. Emotion, cognition, and behavior. Science 2002, 298:1191-1194.
26. Doyle M., Walker R. Curved saccade trajectories: voluntary and reflexive saccades curve away from irrelevant distractors. Exp. Brain Res. 2001, 139:333-344.
27. Dzhelyova M.P., Ellison A., Atkinson A.P. Event-related repetitive TMS reveals distinct, critical roles for right OFA and bilateral posterior STS in Judging the sex and trustworthiness of faces. J. Cogn. Neurosci. 2011, 23:2782-2796.
28. Ellison A., Ball K.L., Moseley P., Dowsett J., Smith D.T., et al. Functional Interaction between right parietal and bilateral frontal cortices during visual search tasks revealed using functional magnetic imaging and transcranial direct current stimulation. PLoS One 2014, 9(4):e93767.
29. Fox E., Lester V., Russo R., Bowles R.J., Pichler A., Dutton K. Facial expressions of emotion: are angry faces detected more efficiently?. Cogn. Emot. 2000, 14:61-92.
30. Fox E., Russo R., Bowles R., Dutton K. Do threatening stimuli draw or hold visual attention in subclinical anxiety?. J. Exp. Psychol.: Gen. 2001, 130:681-700.
31. Fried I., Mateer C., Ojemann G., Wohns R., Fedio P. Organization of visuospatial functions in human cortex. Evidence from electrical stimulation. Brain 1982, 105:349-371.
32. Gandiga P.C., Hummel F.C., Cohen L.G. Transcranial DC stimulation (tDCS): a tool for double-blind sham-controlled clinical studies in brain stimulation. Clin. Neurophysiol. 2006, 117:845-850.
33. Grezes J., Pichon S., de Gelder B. Perceiving fear in dynamic body expressions. NeuroImage 2007, 35:959-967.
34. Halko M.A., Datta A., Plow E.B., Scaturro J., Bikson M., Merabet L.B. Neuroplastic changes following rehabilitative training correlate with regional electrical field induced with tDCS. NeuroImage 2011, 57(3):885-891.
35. 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.
36. Haxby J.V., Hoffman E.A., Gobbini M.I. The distributed human neural system for face perception. Trends Cogn. Sci. 2000, 4:223-233.
37. Hopfinger J.B., Buonocore M.H., Mangun G.R. The neural mechanisms of top-down attentional control. Nat. Neurosci. 2000, 3:284-291.
38. Hsu T.-Y., Tseng L.-Y., Yu J.-X., Kuo W.-J., Hung D.L., Tzeng O.J.L., Walsh V., Muggleton N.G., Juan C.-H. Modulating inhibitory control with direct current stimulation of the superior medial frontal cortex. NeuroImage 2011, 56:2249-2257.
39. Hsu T.Y., Tseng P., Liang W.K., Cheng S.K., Juan C.H. Transcranial direct current stimulation over right posterior parietal cortex changes prestimulus alpha oscillation in visual short-term memory task. NeuroImage 2014, 98:306-313.
40. Jang S.H., Ahn S.H., Byun W.M., Kim C.S., Lee M.Y., Kwon Y.H. The effect of transcranial direct current stimulation on the cortical activation by motor task in the human brain: an fMRI study. Neurosci. Lett. 2009, 460(2):117-120.
41. Jiang Y., He S. Cortical responses to invisible faces: dissociating subsystems for facial-information processing. Curr. Biol. 2006, 16:2023-2029.
42. Juan C.-H., Muggleton N.G., Tzeng O.J.L., Hung D.L., Cowey A., Walsh V. Segregation of visual selection and saccades in human frontal eye fields. Cereb. Cortex 2008, 18:2410-2415.
43. Juan C.H., Shorter-Jacobi S.M., Schall J.D. Dissociation of spatial attention and saccade preparation. Proc. Natl. Acad. Sci. USA 2004, 101:15541-15544.
44. Keeser D., Meindl T., Bor J., Palm U., Pogarell O., Mulert C., Padberg F. Prefrontal transcranial direct current stimulation changes connectivity of resting-state networks during fMRI. J. Neurosci. 2011, 31(43):15284-15293.
45. LeDoux J.E. Emotion circuits in the brain. Annu. Rev. Neurosci. 2000, 23:155-184.
46. Liang W.K., Juan C.H. Modulation of motor control in saccadic behaviors by TMS over the posterior parietal cortex. J. Neurophysiol. 2012, 108(3):741-752.
47. Liu C.L., Tseng P., Chiau H.Y., Liang W.K., Hung D.L., Tzeng O.J., Muggleton N.G., Juan C.H. The location probability effects of saccade reaction times are modulated in the frontal eye fields but not in the supplementary eye field. Cereb. Cortex 2011, 21:1416-1425.
48. Liversedge S.P., Findlay J.M. Saccadic eye movements and cognition. Trends Cogn. Sci. 2000, 4:6-14.
49. Mattavelli, G., Sormaz, M., Flack, T., Asghar, A. U., Fan, S., Frey, J., & Andrews, T. J., 2013. Neural responses to facial expressions support the role of the amygdala in processing threat. Social cognitive and affective neuroscience. http://dx.doi.org/10.1093/scan/nst162.
50. McCreery D.B., Agnew W.F., Yuen T.G., Bullara L. Charge density and charge per phase as cofactors in neural injury induced by electrical stimulation. IEEE Trans. Biomed. Eng. 1990, 37(10):996-1001.
51. McNeil J.E., Warrington E.K. Prosopagnosia: a face-specific disorder. Q. J. Exp. Psychol. A 1993, 46:1-10.
52. McPeek R.M. Incomplete suppression of distractor-related activity in the frontal eye field results in curved saccades. J. Neurophysiol. 2006, 96:2699-2711.
53. McSorley E., Haggard P., Walker R. Time course of oculomotor inhibition revealed by saccade trajectory modulation. J. Neurophysiol. 2006, 96:1420-1424.
54. Mogg K., Bradley B.P. Orienting of attention to threatening facial expressions presented under conditions of restricted awareness. Cogn. Emot. 1999, 13:713-740.
55. Morris A.P., Chambers C.D., Mattingley J.B. Parietal stimulation destabilizes spatial updating across saccadic eye movements. Proc. Natl. Acad. Sci. USA 2007, 104:9069-9074.
56. Muggleton N.G., Chen C.-Y., Tzeng O.J.L., Hung D.L., Juan C.-H. Inhibitory control and the frontal eye fields. J. Cogn. Neurosci. 2010, 22:2804-2812.
57. Muggleton N.G., Juan C.-H., Cowey A., Walsh V. Human frontal eye fields and visual search. J. Neurophysiol. 2003, 89:3340-3343.
58. Narumoto J., Okada T., Sadato N., Fukui K., Yonekura Y. Attention to emotion modulates fMRI activity in human right superior temporal sulcus. Brain Res. Cogn. Brain Res. 2001, 12:225-231.
59. Nitsche M.A., Boggio P.S., Fregni F., Pascual-Leone A. Treatment of depression with transcranial direct current stimulation (tDCS): a review. Exp. Neurol. 2009, 219:14-19.
60. Nitsche M.A., Paulus W. Excitability changes induced in the human motor cortex by weak transcranial direct current stimulation. J. Physiol. 2000, 527(Pt 3):633-639.
61. Nitsche M.A., Schauenburg A., Lang N., Liebetanz D., Exner C., Paulus W., Tergau F. Facilitation of implicit motor learning by weak transcranial direct current stimulation of the primary motor cortex in the human. J. Cogn. Neurosci. 2003, 15:619-626.
62. Nobre A.C., Coull J.T., Maquet P., Frith C.D., Vandenberghe R., Mesulam M.M. Orienting attention to locations in perceptual versus mental representations. J. Cogn. Neurosci. 2004, 16:363-373.
63. Nummenmaa L., Hyönä J., Calvo M.G. Emotional scene content drives the saccade generation system reflexively. J. Exp. Psychol.: Hum. Percept. Perform. 2009, 35:305-323.
64. Nummenmaa L., Hyona J., Calvo M.G. Eye movement assessment of selective attentional capture by emotional pictures. Emotion 2006, 6:257-268.
65. Pessoa L. On the relationship between emotion and cognition. Nat. Rev. Neurosci. 2008, 9:148-158.
66. Pessoa L., McKenna M., Gutierrez E., Ungerleider L.G. Neural processing of emotional faces requires attention. Proc. Natl. Acad. Sci. USA 2002, 99:11458-11463.
67. Pessoa L., Ungerleider L.G. Neuroimaging studies of attention and the processing of emotion-laden stimuli. Prog. Brain Res. 2004, 144:171-182.
68. Phelps E.A. Emotion and cognition: insights from studies of the human amygdala. Annu. Rev. Psychol. 2006, 57:27-53.
69. Pereira J.B., Junqué C., Bartrés-Faz D., Martí M.J., Sala-Llonch R., Compta Y., Tolosa E. Modulation of verbal fluency networks by transcranial direct current stimulation (tDCS) in Parkinson[U+05F3]s disease. Brain Stimul. 2013, 6(1):16-24.
70. Pourtois G., Sander D., Andres M., Grandjean D., Reveret L., Olivier E., Vuilleumier P. Dissociable roles of the human somatosensory and superior temporal cortices for processing social face signals. Eur. J. Neurosci. 2004, 20:3507-3515.
71. Prime S.L., Vesia M., Crawford J.D. Transcranial magnetic stimulation over posterior parietal cortex disrupts transsaccadic memory of multiple objects. J. Neurosci. 2008, 28:6938-6949.
72. Prime S.L., Vesia M., Crawford J.D. TMS over human frontal eye fields disrupts trans-saccadic memory of multiple objects. Cereb. Cortex 2010, 20:759-772.
73. Rudebeck P.H., Bannerman D.M., Rushworth M.F. The contribution of distinct subregions of the ventromedial frontal cortex to emotion, social behavior, and decision making. Cogn. Affect. Behav. Neurosci. 2008, 8:485-497.
74. Rudebeck P.H., Walton M.E., Millette B.H., Shirley E., Rushworth M.F., Bannerman D.M. Distinct contributions of frontal areas to emotion and social behaviour in the rat. Eur. J. Neurosci. 2007, 26:2315-2326.
75. Rushworth M.F., Behrens T.E., Rudebeck P.H., Walton M.E. Contrasting roles for cingulate and orbitofrontal cortex in decisions and social behaviour. Trends Cogn. Sci. 2007, 11:168-176.
76. Rushworth M.F., Taylor P.C. TMS in the parietal cortex: updating representations for attention and action. Neuropsychologia 2006, 44:2700-2716.
77. Rushworth M.F.S., Ellison A., Walsh V. Complementary localization and lateralization of orienting and motor attention. Nat. Neurosci. 2001, 4:656-661.
78. Stagg C.J., Best J.G., Stephenson M.C., O'Shea J., Wylezinska M., Kincses Z.T., Morris P.G., Matthews P.M., Johansen-Berg H. Polarity-sensitive modulation of cortical neurotransmitters by transcranial stimulation. J. Neurosci. 2009, 29:5202-5206.
79. Stein T., Zwickel J., Ritter J., Kitzmantel M., Schneider W.X. The effect of fearful faces on the attentional blink is task dependent. Psychon. Bull. Rev. 2009, 16:104-109.
80. Takano Y., Yokawa T., Masuda A., Niimi J., Tanaka S., Hironaka N. A rat model for measuring the effectiveness of transcranial direct current stimulation using fMRI. Neurosci. Lett. 2011, 491(1):40-43.
81. Taylor P.C.J., Nobre A.C., Rushworth M.F.S. FEF TMS affects visual cortical activity. Cereb. Cortex 2007, 17:391-399.
82. Tseng P., Hsu T.Y., Chang C.F., Tzeng O.J., Hung D.L., Muggleton N.G., Walsh V., Liang W.K., Cheng S.K., Juan C.H. Unleashing potential: tDCS over the right posterior parietal cortex improves change detection in low-performing individuals. J. Neurosci. 2012, 32:10554-10561.
83. Tseng P., Chang C.F., Chiau H.Y., Liang W.K., Liu C.L., Hsu T.Y., Hung D.L., Tzeng O.J.L., Juan C.H. The dorsal attentional system in oculomotor learning of predictive information. Front. Neurosci. 2013, 7:404.
84. Van der Stigchel S. Recent advances in the study of saccade trajectory deviations. Vis. Res. 2010, 50:1619-1627.
85. Van der Stigchel S., Meeter M., Theeuwes J. Eye movement trajectories and what they tell us. Neurosci. Biobehav. Rev. 2006, 30:666-679.
86. Van der Stigchel S., Theeuwes J. Relation between saccade trajectories and spatial distractor locations. Brain Res. Cogn. Brain Res. 2005, 25:579-582.
87. Van der Stigchel S., Theeuwes J. Our eyes deviate away from a location where a distractor is expected to appear. Exp. Brain Res. 2006, 169:338-349.
88. Vuilleumier P. How brains beware: neural mechanisms of emotional attention. Trends Cogn. Sci. 2005, 9:585-594.
89. 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, 30:829-841.
90. Vuilleumier P., Driver J. Modulation of visual processing by attention and emotion: windows on causal interactions between human brain regions. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2007, 362:837-855.
91. Vuilleumier P., Pourtois G. Distributed and interactive brain mechanisms during emotion face perception: evidence from functional neuroimaging. Neuropsychologia 2007, 45(1):174-194.
92. Vuilleumier P., Schwartz S. Beware and be aware: Capture of spatial attention by fear-related stimuli in neglect. Neuroreport 2001, 12(6):1119-1122.
93. Walker R., Techawachirakul P., Haggard P. Frontal eye field stimulation modulates the balance of salience between target and distractors. Brain Res. 2009, 1270:54-63.
94. Xue G., Juan C.H., Chang C.F., Lu Z.L., Dong Q. Lateral prefrontal cortex contributes to maladaptive decisions. Proc. Natl. Acad. Sci. USA 2012, 109(12):4401-4406.
95. Yantis S., Jonides J. Abrupt visual onsets and selective attention: evidence from visual search. J. Exp. Psychol.: Hum. Percept. Perform. 1984, 10:601-621.
96. Yuen T.G., Agnew W.F., Bullara L.A., Jacques S., McCreery D.B. Histological evaluation of neural damage from electrical stimulation: considerations for the selection of parameters for clinical application. Neurosurgery 1981, 9(3):292-299.
97. Zheng X., Alsop D.C., Schlaug G. Effects of transcranial direct current stimulation (tDCS) on human regional cerebral blood flow. NeuroImage 2011, 58(1):26-33.