A common neural code for perceived and inferred emotion

Journal of Neuroscience

Volumn 34, Issue 48, 2014, Pages 15997-16008

  Skerry, Amy E ^a   Saxe, Rebecca ^b  

^a HARVARD UNIVERSITY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Abstraction; Concepts; Emotion attribution; Multimodal; Social cognition; Theory of mind

Indexed keywords

ADULT; ARTICLE; BOLD SIGNAL; BRAIN REGION; CENTRAL PATTERN GENERATOR; CODING; EMOTION; EXPERIMENTAL BEHAVIORAL TEST; FACE PERCEPTION LOCALIZER; FACIAL EXPRESSION; FEMALE; FOLLOW UP; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN EXPERIMENT; MALE; NERVE POTENTIAL; NERVE STIMULATION; NEURAL CODE; NEUROPHYSIOLOGICAL MONITORING; PERCEPTION; PILOT STUDY; PREFRONTAL CORTEX; REWARD; SOCIAL COGNITION; SUPERIOR TEMPORAL SULCUS; TASK PERFORMANCE; THEORY OF MIND; BRAIN; CONTROLLED STUDY; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; PROCEDURES; PSYCHOMOTOR PERFORMANCE; RANDOMIZED CONTROLLED TRIAL; YOUNG ADULT;

ADULT; BRAIN; EMOTIONS; FEMALE; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; NERVE NET; PHOTIC STIMULATION; PILOT PROJECTS; PSYCHOMOTOR PERFORMANCE; YOUNG ADULT;

EID: 84911935038     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1676-14.2014     Document Type: Article

References (89)

1. Adolphs R (2002) Neural systems for recognizing emotion. Curr Opin Neu-robiol 12:169–177.
2. Amodio DM, Frith CD (2006) Meeting of minds: the medial frontal cortex and social cognition. Nat Rev Neurosci 7:268–277.
3. Anzellotti S, Fairhall SL, Caramazza A (2013) Decoding representations of face identity that are tolerant to rotation. Cereb Cortex 24:1988–1995.
4. Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E (2001) The Autism-Spectrum Quotient (AQ): evidence from Asperger syndrome/ high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 31:5–17.
5. Bartra O, McGuire JT, Kable JW (2013) The valuation system: a coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value. Neuroimage 76:412–427.
6. Bestmann S, Ruff CC, Blankenburg F, Weiskopf N, Driver J, Rothwell JC (2008) Mapping causal interregional influences with concurrent TMS– fMRI. Exp Brain Res 191:383–402.
7. Bruneau EG, Pluta A, Saxe R (2012) Distinct roles of the “shared pain” and “theory of mind” networks in processing others’ emotional suffering. Neuropsychologia 50:219–231.
8. Calder AJ, Beaver JD, Winston JS, Dolan RJ, Jenkins R, Eger E, Henson RN (2007) Separate coding of different gaze directions in the superior tem poral sulcus and inferior parietal lobule. Curr Biol 17:20–25.
9. Carey S (1985) Conceptual change in childhood. Cambridge, MA: MIT.
10. Carlin JD, Calder AJ, Kriegeskorte N, Nili H, Rowe JB (2011) A head view-invariant representation of gaze direction in anterior superior temporal sulcus. Curr Biol 21:1817–1821.
11. Chang C, Lin C (2011) LIBSVM: a library for support vector machines. ACM Trans Intellig Sys Tech 2:1–27.
12. Chib VS, Rangel A, Shimojo S, O’Doherty JP (2009) Evidence for acommon representation of decision values for dissimilar goods in human ventro-medial prefrontal cortex. J Neurosci 29:12315–12320.
13. Chikazoe J, Lee DH, Kriegeskorte N, Anderson AK (2014) Population coding of affect across stimuli, modalities and individuals. Nat Neurosci 17: 1114–1122.
14. Clithero JA, Rangel A (2013) Informatic parcellation of the network involved in the computation of subjective value. Soc Cogn Affect Neurosci 9:1289–1302.
15. Davis MH (1983) Measuring individual differences in empathy: evidence for a multidimensional approach. J Pers Soc Psychol 44:113–126.
16. De Martino F, Valente G, Staeren N, Ashburner J, Goebel R, Formisano E (2008) Combining multivariate voxel selection and support vector ma chines for mapping and classification of fMRI spatial patterns. Neuroimage 43:44–58.
17. Devereux BJ, Clarke A, Marouchos A, Tyler LK (2013) Representational similarity analysis reveals commonalities and differences in the semantic processing of words and objects. J Neurosci 33:18906–18916.
18. DiCarlo JJ, Cox DD (2007) Untangling invariant object recognition. Trends Cogn Sci 11:333–341.
19. DiCarlo JJ, Zoccolan D, Rust NC (2012) How does the brain solve visual object recognition? Neuron 73:415–434.
20. Dodell-Feder D, Koster-Hale J, Bedny M, Saxe R (2011) fMRI item analysis in a theory of mind task. Neuroimage 55:705–712.
21. Dufour N, Redcay E, Young L, Mavros PL, Moran JM, Triantafyllou C, Ga-brieli JD, Saxe R (2013) Similar brain activation during false belief tasks in a large sample of adults with and without autism. PLoS One 8:e75468.
22. Ekman P, Rosenberg EL (1997) What the face reveals: basic and applied studies of spontaneous expression using the Facial Action Coding System (FACS). Oxford: Oxford UP.
23. Ethofer T, Anders S, Erb M, Herbert C, Wiethoff S, Kissler J, Grodd W, Wildgruber D (2006) Cerebral pathways in processing of affective prosody: a dynamic causal modeling study. Neuroimage 30:580–587.
24. Etkin A, Egner T, Kalisch R (2011) Emotional processing in anterior cingu-late and medial prefrontal cortex. Trends Cogn Sci 15:85–93.
25. Fairhall SL, Caramazza A (2013) Brain regions that represent amodal conceptual knowledge. J Neurosci 33:10552–10558.
26. Fox CJ, Moon SY, Iaria G, Barton JJ (2009) The correlates of subjective perception of identity and expression in the face network: an fMRI adaptation study. Neuroimage 44:569–580.
27. Freeman J, Brouwer GJ, Heeger DJ, Merriam EP (2011) Orientation decoding depends on maps, not columns. J Neurosci 31:4792–4804.
28. Friston KJ, Harrison L, Penny W (2003) Dynamic causal modelling. Neuro-image 19:1273–1302.
29. Furl N, Hadj-Bouziane F, Liu N, Averbeck BB, Ungerleider LG (2012) Dynamic and static facial expressions decoded from motion-sensitive areas in the macaque monkey. J Neurosci 32:15952–15962.
30. Fusar-Poli P, Placentino A, Carletti F, Landi P, Allen P, Surguladze S, Bene-detti F, Abbamonte M, Gasparotti R, Barale F, Perez J, McGuire P, Politi P (2009) Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci 34:418–432.
31. Goldman AI, Sripada CS (2005) Simulationist models of face-based emotion recognition. Cognition 94:193–213.
32. Gopnik A, Wellman HM (1992) Why the child’s theory of mind really is a theory. Mind Lang 7:145–171.
33. Gothard KM, Battaglia FP, Erickson CA, Spitler KM, Amaral DG (2007) Neural responses to facial expression and face identity in the monkey amygdala. J Neurophysiol 97:1671–1683.
34. Hadj-Bouziane F, Liu N, Bell AH, Gothard KM, Luh WM, Tootell RB, Murray EA, Ungerleider LG (2012) Amygdala lesions disrupt modulation of functional MRI activity evoked by facial expression in the monkey inferior temporal cortex. Proc Natl Acad Sci U S A 109:E3640–E3648.
35. Harmer CJ, Thilo KV, Rothwell JC, Goodwin GM (2001) Transcranial magnetic stimulationof medial–frontal cortex impairs the processingof angry facial expressions. Nat Neurosci 4:17–18.
36. Harry B, Williams MA, Davis C, Kim J (2013) Emotional expressions evoke a differential response in the fusiform face area. Front Hum Neurosci 7:692.
37. Haxby JV, Gobbini MI, Furey ML, Ishai A, Schouten JL, Pietrini P (2001) Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science 293:2425–2430.
38. Hung CP, Kreiman G, Poggio T, DiCarlo JJ (2005) Fast readout of object identity from macaque inferior temporal cortex. Science 310:863–866.
39. Hynes CA, Baird AA, Grafton ST (2006) Differential roleof the orbital frontal lobe in emotional versus cognitive perspective-taking. Neuropsycho-logia 44:374–383.
40. Julian JB, Fedorenko E, Webster J, Kanwisher N (2012) An algorithmic method for functionally defining regions of interest in the ventral visual pathway. Neuroimage 60:2357–2364.
41. Kable JW, Glimcher PW (2007) The neural correlates of subjective value during intertemporal choice. Nat Neurosci 10:1625–1633.
42. Kamitani Y, Tong F (2005) Decoding the visual and subjective contents of the human brain. Nat Neurosci 8:679–685.
43. Kanwisher N, Yovel G (2006) The fusiform face area: a cortical region specialized for the perception of faces. Philos Trans R Soc Lond B Biol Sci 361:2109–2128.
44. Kaufman A (1990) KBIT-2: Kaufman Brief Intelligence Test. Bloomington, MN: NCS Pearson.
45. Kreifelts B, Ethofer T, Shiozawa T, Grodd W, Wildgruber D (2009) Cerebral representation of non-verbal emotional perception: fMRI reveals audiovisual integration area between voice- and face-sensitive regions in the superior temporal sulcus. Neuropsychologia 47:3059–3066.
46. Kriegeskorte N, Kievit RA (2013) Representational geometry: integrating cognition, computation, and the brain. Trends Cogn Sci 17:401–412.
47. Kriegeskorte N, Goebel R, Bandettini P (2006) Information-based functional brain mapping. Proc Natl Acad Sci U S A 103:3863–3868.
48. Lin A, Adolphs R, Rangel A (2012) Social and monetary reward learning engage overlapping neural substrates. Soc Cogn Affect Neurosci 7:274–281.
49. Lindquist KA, Wager TD, Kober H, Bliss-Moreau E, Barrett LF (2012) The brain basis of emotion: a meta-analytic review. Behav Brain Sci 35:121–143.
50. Mattavelli G, Cattaneo Z, Papagno C (2011) Transcranial magnetic stimulation of medial prefrontal cortex modulates face expressions processing in a priming task. Neuropsychologia 49:992–998.
51. Mitchell JP (2009) Inferences about mental states. Philos Trans R Soc Lond B Biol Sci 364:1309–1316.
52. Mitchell TM, Hutchinson R, Niculescu RS, Pereira F, Wang X, Just M, Newman S (2004) Learning to decode cognitive states from brain images. Mach Learn 57:145–175.
53. Niedenthal PM (2007) Embodying emotion. Science 316:1002–1005.
54. Norman KA, Polyn SM, Detre GJ, Haxby JV (2006) Beyond mind-reading: multi-voxel pattern analysis of fMRI data. Trends Cogn Sci 10:424–430.
55. Oosterhof NN, Todorov A (2009) Shared perceptual basis of emotional expressions and trustworthiness impressions from faces. Emotion 9:128–133.
56. Op de Beeck HP (2010) Against hyperacuity in brain reading: spatial smoothing does not hurt multivariate fMRI analyses? Neuroimage 49: 1943–1948.
57. Ortony A (1990) Reactions to Events I. In: The cognitive structure of emotions. p 228. Cambridge, UK: Cambridge UP.
58. Peelen MV, Atkinson AP, Vuilleumier P (2010) Supramodal representations of perceived emotions in the human brain. J Neurosci 30:10127–10134.
59. Pelphrey KA, Morris JP, Michelich CR, Allison T, McCarthy G (2005) Functional anatomy of biological motion perception in posterior temporal cortex: an fMRI study of eye, mouth and hand movements. Cereb Cortex 15:1866–1876.
60. Pereira F, Mitchell T, Botvinick M (2009) Machine learning classifiers and fMRI: a tutorial overview. Neuroimage 45:S199–S209.
61. Pessoa L, Adolphs R (2010) Emotion processing and the amygdala: from a “low road” to “many roads” of evaluating biological significance. Nat Rev Neurosci 11:773–783.
62. Pitcher D (2014) Facial expression recognition takes longer in the posterior superior temporal sulcus than in the occipital face area. J Neurosci 34: 9173–9177.
63. Pitcher D, Dilks DD, Saxe RR, Triantagyllou C, Kanwisher N (2011) Differential selectivity for dynamic versus static information in face selective cortical regions. Neuroimage 56:2356–2363.
64. Plassmann H, O’Doherty J, Rangel A (2007) Orbitofrontal cortex encodes willingness to pay in everyday economic transactions. J Neurosci 27: 9984–9988.
65. Ruff CC, Fehr E (2014) The neurobiology of rewards and values in social decision making. Nat Rev Neurosci 15:549–562.
66. Said CP, Moore CD, Engell AD, Todorov A, Haxby JV (2010a) Distributed representations of dynamic facial expressions in the superior temporal sulcus. J Vis 10:11.
67. Said CP, Moore CD, Norman KA, Haxby JV, Todorov A (2010b) Graded representations of emotional expressions in the left superior temporal sulcus. Front Syst Neurosci 4:6.
68. Saxe R, Kanwisher N (2003) People thinking about thinking people. The role of the temporo-parietal junction in “theory of mind.” Neuroimage 19:1835–1842.
69. Scherer KR, Meuleman B (2013) Human emotion experiences can be predicted on theoretical grounds: evidence from verbal labeling. PLoS One 8:e58166.
70. Seung HS, Sompolinsky H (1993) Simple models for reading neuronal population codes. Proc Natl Acad Sci U S A 90:10749–10753.
71. Shamay-Tsoory SG, Tomer R, Berger BD, Aharon-Peretz J (2003) Characterization of empathy deficits following prefrontal brain damage: the role of the right ventromedial prefrontal cortex. J Cogn Neurosci 15:324–337.
72. Shamay-Tsoory SG, Aharon-Peretz J, Perry D (2009) Two systems for empathy: a double dissociation between emotional and cognitive empathy in inferior frontal gyrus versus ventromedial prefrontal lesions. Brain 132: 617–627.
73. Shamir M, Sompolinsky H (2006) Implications of neuronal diversity on population coding. Neural Comput 18:1951–1986.
74. Simmons JP, Nelson LD, Simonsohn U (2011) False-positive psychology undisclosed flexibility in data collection and analysis allows presenting anything as significant. Psychol Sci 22:1359–1366.
75. Singer T, Critchley HD, Preuschoff K (2009) A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13:334–340.
76. Spunt RP, Lieberman MD (2012) An integrative model of the neural systems supporting the comprehension of observed emotional behavior. Neuroimage 59:3050–3059.
77. Stelzer J, Chen Y, Turner R (2013) Statistical inference and multiple testing correction in classification-based multi-voxel pattern analysis (MVPA): random permutations and cluster size control. Neuroimage 65:69–82.
78. Stevenson RA, James TW (2009) Audiovisual integration in human superior temporal sulcus: inverse effectiveness and the neural processing of speech and object recognition. Neuroimage 44:1210–1223.
79. Tanaka K (1993) Neuronal mechanisms of object recognition. Science 262: 685–688.
80. Tversky A, Kahneman D (1991) Loss aversion inriskless choice:areference-dependent model. Q J Econ 106:1039–1061.
81. Ullman S (1998) Three-dimensional object recognition based on the combination of views. Cognition 67:21–44.
82. Völlm BA, Taylor AN, Richardson P, Corcoran R, Stirling J, McKie S, Deakin JF, Elliott R (2006) Neuronal correlates of theory of mind and empathy: a functional magnetic resonance imaging study in a nonverbal task. Neu-roimage 29:90–98.
83. Winecoff A, Clithero JA, Carter RM, Bergman SR, Wang L, Huettel SA (2013) Ventromedial prefrontal cortex encodes emotional value. J Neu-rosci 33:11032–11039.
84. Xu X, Biederman I (2010) Loci of the release from fMRI adaptation for changesin facial expression, identity, and viewpoint. JVis 10:36.
85. Zaki J, Ochsner KN (2009) The need for a cognitive neuroscience of naturalistic social cognition. Ann N Y Acad Sci 1167:16–30.
86. Zaki J, Bolger N, Ochsner K (2008) It takes two: the interpersonal nature of empathic accuracy. Psychol Sci 19:399–404.
87. Zaki J, Weber J, Bolger N, Ochsner K (2009a) The neural bases of empathic accuracy. Proc Natl Acad Sci U S A 106:11382–11387.
88. Zaki J, Bolger N, Ochsner K (2009b) Unpacking the informational bases of empathic accuracy. Emotion 9:478–487.
89. Zaki J, Hennigan K, Weber J, Ochsner KN (2010) Social cognitive conflict resolution: contributions of domain-general and domain-specific neural systems. J Neurosci 30:8481–8488.