Identifying Emotions on the Basis of Neural Activation
Karim S Kassam, Amanda R Markey, Vladimir L Cherkassky, George Loewenstein, Marcel Adam Just, Karim S Kassam, Amanda R Markey, Vladimir L Cherkassky, George Loewenstein, Marcel Adam Just
Abstract
We attempt to determine the discriminability and organization of neural activation corresponding to the experience of specific emotions. Method actors were asked to self-induce nine emotional states (anger, disgust, envy, fear, happiness, lust, pride, sadness, and shame) while in an fMRI scanner. Using a Gaussian Naïve Bayes pooled variance classifier, we demonstrate the ability to identify specific emotions experienced by an individual at well over chance accuracy on the basis of: 1) neural activation of the same individual in other trials, 2) neural activation of other individuals who experienced similar trials, and 3) neural activation of the same individual to a qualitatively different type of emotion induction. Factor analysis identified valence, arousal, sociality, and lust as dimensions underlying the activation patterns. These results suggest a structure for neural representations of emotion and inform theories of emotional processing.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
References
- Clore G, Huntsinger J (2007) How emotions inform judgment and regulate thought. Trends Cogn. Sci. (Regul. Ed.) 11(9): 393–399.
- Damasio AR (1994) Descartes’ Error: Emotion, Reason and the Human Brain. Kirkwood, NY: Putnam Publishing.
- Overskeid G (2000) The slave of the passions: Experiencing problems and selecting solutions. Rev Gen Psychol 4(3): 284–308.
- Lerner JS, Keltner D (2001) Fear, anger, and risk. J Pers Soc Psychol 81(1): 146.
- Phelps EA (2004) Human emotion and memory:interactions of the amygdala and hippocampal complex. Curr. Opin. Neurobiol. 14: 198–202.
- Phelps EA, Ling S, Carrasco M (2006) Emotion facilitates perception and potentiates the perceptual benefits of attention. Psychol Sci 17(4): 292–299.
- Scott SK, Young AW, Calder AJ, Hellawell DJ, Aggleton JP, et al. (1997) Impaired auditory recognition of fear and anger following bilateral amygdala lesions. Nature 385: 254–257.
- Barrett LF (2006) Are emotions natural kinds? Perspect Psychol Sci 1: 28–58.
- Izard CE (2007) Basic emotions, natural kinds, emotion schemas and a new paradigm. Perspect Psychol Sci 2: 260–280.
- Panksepp J (2007) Neurologizing the psychology of affects: How appraisal-based constructivism and basic emotion theory can coexist. Perspect Psychol Sci 2(3): 281–296.
- Cosmides L, Tooby J (2004) Evolutionary Psychology and the Emotions. In: Lewis M, Haviland-Jones JM, editors. Handbook of Emotions. NY: Guilford.
- Scarantino A, Griffiths P (2011) Don’t give up on basic emotions. Emot Rev 3: 444–454.
- Kober H, Barrett LF, Joseph J, Bliss-Moreau E, Lindquist K, et al. (2008) Functional grouping and cortical–subcortical interactions in emotion: A meta-analysis of neuroimaging studies. Neuroimage 42: 998.
- 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.
- Phan K, Wager T, Taylor S, Liberzon I (2002) Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16: 331–348.
- Wager TD, Phan KL, Liberzon I, Taylor SF (2003) Valence, gender, and lateralization of functional brain anatomy in emotion: a meta-analysis of findings from neuroimaging. Neuroimage 19: 513–531.
- Murphy FC, Nimmo-Smith I, Lawrence AD (2003) Functional neuroanatomy of emotions: a meta-analysis. Cogn Affect Behav Neurosci 3: 207–233.
- Vytal K, Hamann S (2010) Neuroimaging support for discrete neural correlates of basic emotions: A voxel- based meta-analysis. J Cogn Neurosci 22: 2864–2885.
- Stemmler G (2003) Introduction: Autonomic psychophysiology. In: Davidson RJ, Scherer KR, Goldsmith HH, editors. Handbook of affective sciences. New York: Oxford University Press. 131–134.
- Jimura K, Poldrack RA (2012) Analyses of regional-average activation and multivoxel pattern information tell complementary stories. Neuropsychologia 50: 544–552.
- Mitchell TM (1997) Mach Learn. WCB.
- Mitchell TM, Hutchinson R, Niculescu RS, Pereira F, Wang X, et al. (2004) Learning to decode cognitive states from brain images. Mach Learn 57: 145–175.
- Kolodyazhniy V, Kreibig SD, Gross JJ, Roth WT, Wilhelm FH (2011) An affective computing approach to physiological emotion specificity: Toward subject-independent and stimulus-independent classification of film-induced emotions. Psychophysiology 48: 908–922.
- Ethofer T, Van De Ville D, Scherer K, Vuilleumier P (2009) Decoding of emotional information in voice-sensitive cortices. Curr Biol 19: 1028–1033.
- Said CP, Moore CD, Engell AD, Haxby JV (2010) Distributed representations of dynamic facial expressions in the superior temporal sulcus. J Vis 10: 1–12.
- Peelen MV, Atkinson AP, Vuilleumier P (2010) Supramodal representations of perceived emotions in the human brain. J Neurosci 30: 10127–10134.
- Baucom LB, Wedell DH, Wang J, Blitzer DN, Shinkareva SV (2012) Decoding the neural representation of affective states. Neuroimage 59: 718–727.
- Lang PJ, Bradley MM, Cuthbert BN (1995) International affective picture system (IAPS): Technical manual and affective ratings. Gainesville, FL: University of Florida, Center for Research in Psychophysiology.
- Anders S, Lotze M, Erb M, Grodd W, Birbaumer N (2004) Brain activity underlying emotional valence and arousal: a response-related fMRI study. Hum Brain Mapp 23: 200–209.
- Nielen MMA, Heslenfeld DJ, Heinen K, Van Strien JW, Witter MP, et al. (2009) Distinct brain systems underlie the processing of valence and arousal of affective pictures. Brain Cogn 71: 387–396.
- Barrett LF, Russell JA (1999) The Structure of Current Affect Controversies and Emerging Consensus. Curr Dir Psychol Sci 8: 10–14.
- Watson D, Tellegen A (1985) Toward a consensual structure of mood. Psychol Bull 98: 219–235.
- Russell JA (1980) A circumplex model of affect. J Pers Soc Psychol 39: 1161–1178.
- Carver CS, Harmon-Jones E (2009) Anger is an approach-related affect: evidence and implications. Psychol Bull 135: 183.
- Britton JC, Phan KL, Taylor SF, Welsh RC, Berridge KC, et al. (2006) Neural correlates of social and nonsocial emotions: An fMRI study. Neuroimage 31: 397–409.
- Keltner D, Kring AM (1998) Emotion, social function, and psychopathology. Rev Gen Psychol 2: 320.
- Frijda NH, Mesquita B (1994) The social roles and functions of emotions. In: Markus HR, Kitayama S, editors. Emotion and Culture. New York: American Psychological Association. 51–87.
- Leary MR (2001) Affect, Cognition, and the Social Emotions. Feeling and thinking: The role of affect in social cognition. In: Forgas JP, editor. Feeling and Thinking: The Role of Affect in Social Cognition. New York: Cambridge University Press. 331–356.
- Adolphs R, Baron-Cohen S, Tranel D (2002) Impaired recognition of social emotions following amygdala damage. J Cogn Neurosci 14: 1264–1274.
- Just MA, Cherkassky VL, Aryal S, Mitchell TM (2010) A neurosemantic theory of concrete noun representation based on the underlying brain codes. PLoS One 5: e8622.
- Mitchell TM, Shinkareva SV, Carlson A, Chang K, Malave VL, et al. (2008) Predicting human brain activity associated with the meanings of nouns. Science 320: 1191–1195.
- Hand DJ, Yu K (2001) Idiot’s Bayes–not so stupid after all? Int Stat Rev 69: 385–398.
- Damarla SR, Just MA (2013) Decoding the representation of numerical values from brain activation patterns. Hum Brain Mapp. In press.
- Lerner JS, Tiedens LZ (2006) Portrait of the angry decision maker: How appraisal tendencies shape anger’s influence on cognition. J Behav Decis Mak 19: 115–137.
- Harmon-Jones E (2003) Clarifying the emotive functions of asymmetrical frontal cortical activity. Psychophysiology 40: 838–848.
- Harmon-Jones E, Harmon-Jones C, Abramson L, Peterson CK (2009) PANAS Positive activation is associated with anger. Emotion 9: 183–196.
- Ekman P (1992) An argument for basic emotions. Cogn Emot 6: 169–200.
- Kaiser HF (1960) The application of electronic computers to factor analysis. Educ Psychol Meas 20: 141–151.
- Horn JL (1965) A rationale and test for the number of factors in factor analysis. Psychometrika 32: 179–185.
- Blair KS, Smith BW, Mitchell DGV, Morton J, Vythilingam M, et al. (2007) Modulation of emotion by cognition and cognition by emotion. Neuroimage 35: 430–440.
- Beauregard M, Levesque J, Bourgouin P (2001) Neural correlates of conscious self-regulation of emotion. J Neurosci 21: 6993–7000.
- Bechara A, Damasio H, Tranel D, Damasio AR (1997) Deciding advantageously before knowing the advantageous strategy. Science 275: 1293–1295.
- Rangel A, Camerer C, Montague PR (2008) A framework for studying the neurobiology of value-based decision making. Nat. Rev. Neurosci. 9: 545–556.
- Rule RR, Shimamura AP, Knight RT (2002) Orbitofrontal cortex and dynamic filtering of emotional stimuli. Cogn Affect Behav Neurosci 2: 264–270.
- Mitchell JP (2008) Contributions of functional neuroimaging to the study of social cognition. Curr Dir Psychol Sci 17: 142–146.
- Kanwisher N, McDermott J, Chun MM (1997) The fusiform face area: A module in human extrastriate cortex specialized for face perception. J. Neurosci. 17: 4302–4311.
- Mouras H, Stoleru S, Bittoun J, Glutron D, Pelegrini-Issac M, et al. (2003) Brain processing of visual sexual stimuli in healthy men: A functional magnetic resonance imaging study. Neuroimage 20: 855–869.
- Lindquist KA, Barrett LF (2012) A functional architecture of the human brain: Emerging insights from the science of emotion. Trends Cogn. Sci. (Regul. Ed.) 16: 533–540.
- Russell J (2003) Core affect and the psychological construction of emotion. Psychol Rev 110: 145–172.
- Lang PJ (1995) The emotion probe: Studies of motivation and attention. Am Psychol 50: 372.
- Loewenstein G (2007) Defining Affect (Commentary on Klaus Scherer’s “What is an Emotion?”. ) Semiotica 46(3): 405–410.
- Robinson MD, Clore GL (2002) Belief and feeling: Evidence for an accessibility model of emotional self-report. Psychol Bull 128: 934–960.
- Winkielman P, Berridge KC (2004) Unconscious emotion. Curr Dir Psychol Sci 13: 120–123.
- LeDoux JE (1996) The emotional brain: The mysterious underpinnings of emotional life. New York: Simon and Schuster.
- Larsen JT, Berntson GG, Poehlmann KM, Ito TA, Cacioppo JT (2008) The psychophysiology of emotion. In: Lewis M, Haviland-Jones JM, Barrett LF, editors. The Handbook of Emotion. New York: Guilford. 180–195.
- Levenson RW (2003) Autonomic specificity and emotion. In: Davidson RJ, Scherer KR, Goldsmith HH, editors. Handbook of Affective Sciences. New York: Oxford University Press. 212–224.
- Ekman P, Friesen WV (1971) Constants across cultures in the face and emotion. J Pers Soc Psychol 17: 124–129.
- Russell JA (1995) Facial expressions of emotion: What lies beyond minimal universality? Psychol Bull 118: 379–379.
- LeDoux JE (2000) Emotion circuits in the brain. Annu. Rev. Neurosci. 23: 155–184.
- Panksepp J (1998) Affective neuroscience: The foundations of human and animal emotions. New York: Oxford University Press.
- Mauss IB, Robinson MD (2009) Measures of emotion: A review. Cogn Emot 23: 209–237.
Source: PubMed