Intersubject variability in fearful face processing: the linkbetween behavior and neural activation

Springer Science and Business Media LLC - Tập 14 - Trang 1438-1453 - 2014
Tracy J. Doty1,2,3, Shruti Japee1, Martin Ingvar2, Leslie G. Ungerleider1
1Laboratory of Brain and Cognition, National Institute of Mental Health, Bethesda, USA
2Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
3Translational Neuroscience Branch, Human Research and Engineering Directorate, United States Army Research Laboratory, Aberdeen Proving Ground, Aberdeen, USA

Tóm tắt

Stimuli that signal threat show considerable variability in the extents to which they enhance behavior, even among healthy individuals. However, the neural underpinning of this behavioral variability is not well understood. By manipulating expectation of threat in an fMRI study of fearful versus neutral face categorization, we uncovered a network of areas underlying variability in threat processing in healthy adults. We explicitly altered expectations by presenting face images at three different expectation levels: 80 %, 50 %, and 20 %. Subjects were instructed to report as quickly and accurately as possible whether the face was fearful (signaled threat) or not. An uninformative cue preceded each face by 4 s. By taking the difference between reaction times (RTs) to fearful and neutral faces, we quantified an overall fear RT bias (i.e., faster to fearful than to neutral faces) for each subject. This bias correlated positively with late-trial fMRI activation (8 s after the face) during unexpected-fearful-face trials in bilateral ventromedial prefrontal cortex, the left subgenual cingulate cortex, and the right caudate nucleus, and correlated negatively with early-trial fMRI activation (4 s after the cue) during expected-neutral-face trials in bilateral dorsal striatum and the right ventral striatum. These results demonstrate that the variability in threat processing among healthy adults is reflected not only in behavior, but also in the magnitude of activation in medial prefrontal and striatal regions that appear to encode affective value.

Tài liệu tham khảo

Arrais, K. C., Machado-de-Sousa, J. P., Trzesniak, C., Santos Filho, A., Ferrari, M. C. F., Osório, F. L., … Crippa, J. A. S. (2010). Social anxiety disorder women easily recognize fearfull, sad and happy faces: The influence of gender. Journal of Psychiatric Research, 44, 535–540. doi:10.1016/j.jpsychires.2009.11.003 Bar-Haim, Y., Lamy, D., Pergamin, L., Bakermans-Kranenburg, M. J., & van IJzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133, 1–24. doi:10.1037/0033-2909.133.1.1 Barlow, D. H. (2004). Anxiety and its disorders: The nature and treatment of anxiety and panic. New York: Guilford Press. Bechara, A., Damasio, A. R., Damasio, H., & Anderson, S. W. (1994). Insensitivity to future consequences following damage to human prefrontal cortex. Cognition, 50, 7–15. Bechara, A., Tranel, D., & Damasio, H. (2000). Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain, 123, 2189–2202. doi:10.1093/brain/123.11.2189 Blair, K., Marsh, A. A., Morton, J., Vythilingam, M., Jones, M., Mondillo, K., & Blair, J. R. (2006). Choosing the lesser of two evils, the better of two goods: Specifying the roles of ventromedial prefrontal cortex and dorsal anterior cingulate in object choice. Journal of Neuroscience, 26, 11379–11386. doi:10.1523/JNEUROSCI.1640-06.2006 Blasi, G., Hariri, A. R., Alce, G., Taurisano, P., Sambataro, F., Das, S., & Mattay, V. S. (2009). Preferential amygdala reactivity to the negative assessment of neutral faces. Biological Psychiatry, 66, 847–853. doi:10.1016/j.biopsych.2009.06.017 Bradley, B. P., Mogg, K., White, J., Groom, C., & de Bono, J. (1999). Attentional bias for emotional faces in generalized anxiety disorder. British Journal of Clinical Psychology, 38, 267–278. Breiter, H. C., Etcoff, N. L., Whalen, P. J., Kennedy, W. A., Rauch, S. L., Buckner, R. L., & Rosen, B. R. (1996). Response and habituation of the human amygdala during visual processing of facial expression. Neuron, 17, 875–887. Carmichael, S. T., & Price, J. L. (1995). Limbic connections of the orbital and medial prefrontal cortex in macaque monkeys. Journal of Comparative Neurology, 363, 615–641. doi:10.1002/cne.903630408 Carmichael, S. T., & Price, J. L. (1996). Connectional networks within the orbital and medial prefrontal cortex of macaque monkeys. Journal of Comparative Neurology, 371, 179–207. Caseras, X., Àvila, C., & Torrubia, R. (2003). The measurement of individual differences in Behavioural Inhibition and Behavioural Activation Systems: A comparison of personality scales. Personality and Individual Differences, 34, 999–1013. doi:10.1016/S0191-8869(02)00084-3 Chawla, D., Rees, G., & Friston, K. J. (1999). The physiological basis of attentional modulation in extrastriate visual areas. Nature Neuroscience, 2, 671–676. Cloninger, C. R., Przybeck, T. R., & Svrakic, D. M. (1991). The tridimensional personality questionnaire: U.S. normative data. Psychological Reports, 69, 1047–1057. Costa, P. T., & McCrae, R. R. (1992). Revised NEO Personality Inventory (NEO PI-R) and NEO Five-Factor Inventory (NEO FFI): Professional manual. Odessa: Psychological Assessment Resources. Costafreda, S. G., Brammer, M. J., David, A. S., & Fu, C. H. Y. (2008). Predictors of amygdala activation during the processing of emotional stimuli: A meta-analysis of 385 PET and fMRI studies. Brain Research Reviews, 58, 57–70. doi:10.1016/j.brainresrev.2007.10.012 Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29, 162–173. Critchley, H. D., Elliott, R., Mathias, C. J., & Dolan, R. J. (2000). Neural activity relating to generation and representation of galvanic skin conductance responses: A functional magnetic resonance imaging study. Journal of Neuroscience, 20, 3033–3040. Dale, A. M. (1999). Optimal experimental design for event-related fMRI. Human Brain Mapping, 8, 109–114. Davidson, R. J., Maxwell, J. S., & Shackman, A. J. (2004). The privileged status of emotion in the brain. Proceedings of the National Academy of Sciences, 101, 11915–11916. doi:10.1073/pnas.0404264101 Deane, G. E. (1969). Cardiac activity during experimentally induced anxiety. Psychophysiology, 6, 17–30. Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Shehzad, Z., … Milham, M. P. (2008). Functional connectivity of human striatum: A resting state FMRI study. Cerebral Cortex, 18, 2735–2747. doi:10.1093/cercor/bhn041 Doty, T. J., Japee, S., Ingvar, M., & Ungerleider, L. G. (2013). Fearful face detection sensitivity in healthy adults correlates with anxiety-related traits. Emotion, 13, 183–188. doi:10.1037/a0031373 Epstein, S. (1972). The nature of anxiety with emphasis upon its relationship to expectancy. In C. D. Spielberger (Ed.), Anxiety: Current trends in theory and research (Vol. 2, pp. 292–338). New York: Academic Press. Epstein, S., & Roupenian, A. (1970). Heart rate and skin conductance during experimentally induced anxiety: The effect of uncertainty about receiving a noxious stimulus. Journal of Personality and Social Psychology, 16, 20–28. Fox, E. (2002). Processing emotional facial expressions: The role of anxiety and awareness. Cognitive, Affective, & Behavioral Neuroscience, 2, 52–63. doi:10.3758/CABN.2.1.52 Fox, E., Lester, V., Russo, R., Bowles, R. J., Pichler, A., & Dutton, K. (2000). Facial expressions of emotion: Are angry faces detected more efficiently? Cognition and Emotion, 14, 61–92. doi:10.1080/026999300378996 Furmark, T., Tillfors, M., Marteinsdottir, I., Fischer, H., Pissiota, A., Långström, B., & Fredrikson, M. (2002). Common changes in cerebral blood flow in patients with social phobia treated with citalopram or cognitive–behavioral therapy. Archives of General Psychiatry, 59, 425–433. Haber, S. N., Kunishio, K., Mizobuchi, M., & Lynd-Balta, E. (1995). The orbital and medial prefrontal circuit through the primate basal ganglia. Journal of Neuroscience, 15, 4851–4867. Hansen, C. H., & Hansen, R. D. (1988). Finding the face in the crowd: An anger superiority effect. Journal of Personality and Social Psychology, 54, 917–924. Hikosaka, O., Sakamoto, M., & Usui, S. (1989). Functional properties of monkey caudate neurons: III. Activities related to expectation of target and reward. Journal of Neurophysiology, 61, 814–832. Ishai, A., Pessoa, L., Bikle, P. C., & Ungerleider, L. G. (2004). Repetition suppression of faces is modulated by emotion. Proceedings of the National Academy of Sciences, 101, 9827–9832. doi:10.1073/pnas.0403559101 Japee, S., Crocker, L., Carver, F., Pessoa, L., & Ungerleider, L. G. (2009). Individual differences in valence modulation of face-selective M170 response. Emotion, 9, 59–69. doi:10.1037/a0014487 Johansen-Berg, H., Gutman, D. A., Behrens, T. E. J., Matthews, P. M., Rushworth, M. F. S., Katz, E., … Mayberg, H. S. (2008). Anatomical connectivity of the subgenual cingulate region targeted with deep brain stimulation for treatment-resistant depression. Cerebral Cortex, 18, 1374–1383. doi:10.1093/cercor/bhm167 Kastner, S., Pinsk, M. A., De Weerd, P., Desimone, R., & Ungerleider, L. G. (1999). Increased activity in human visual cortex during directed attention in the absence of visual stimulation. Neuron, 22, 751–761. Kim, M. J., Gee, D. G., Loucks, R. A., Davis, F. C., & Whalen, P. J. (2011). Anxiety dissociates dorsal and ventral medial prefrontal cortex functional connectivity with the amygdala at rest. Cerebral Cortex, 21, 1667–1673. doi:10.1093/cercor/bhq237 Kim, M. J., & Whalen, P. J. (2009). The structural integrity of an amygdala–prefrontal pathway predicts trait anxiety. Journal of Neuroscience, 29, 11614–11618. doi:10.1523/JNEUROSCI.2335-09.2009 Knutson, B., Adams, C. M., Fong, G. W., & Hommer, D. (2001). Anticipation of increasing monetary reward selectively recruits nucleus accumbens. Journal of Neuroscience, 21, RC159. Koenigs, M., Young, L., Adolphs, R., Tranel, D., Cushman, F., Hauser, M., & Damasio, A. (2007). Damage to the prefrontal cortex increases utilitarian moral judgements. Nature, 446, 908–911. doi:10.1038/nature05631 Kunishio, K., & Haber, S. N. (1994). Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input. Journal of Comparative Neurology, 350, 337–356. doi:10.1002/cne.903500302 Leh, S. E., Ptito, A., Chakravarty, M. M., & Strafella, A. P. (2007). Fronto-striatal connections in the human brain: A probabilistic diffusion tractography study. Neuroscience Letters, 419, 113–118. doi:10.1016/j.neulet.2007.04.049 Lehéricy, S., Ducros, M., Van de Moortele, P.-F., Francois, C., Thivard, L., Poupon, C., … Kim, D.-S. (2004). Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans. Annals of Neurology, 55, 522–529. doi:10.1002/ana.20030 Lundqvist, D., Flykt, A., & Öhman, A. (1998). The Karolinska directed emotional faces. Solna: Karolinska Institutet, Psychology section, Department of Clinical Neuroscience. Mayberg, H. S., Liotti, M., Brannan, S. K., McGinnis, S., Mahurin, R. K., Jerabek, P. A., … Fox, P. T. (1999). Reciprocal limbic-cortical function and negative mood: Converging PET findings in depression and normal sadness. American Journal of Psychiatry, 156, 675–682. Mogg, K., & Bradley, B. P. (1999). Some methodological issues in assessing attentional biases for threatening faces in anxiety: A replication study using a modified version of the probe detection task. Behaviour Research and Therapy, 37, 595–604. Morris, J. S., Friston, K. J., Büchel, C., Frith, C. D., Young, A. W., Calder, A. J., & Dolan, R. J. (1998). A neuromodulatory role for the human amygdala in processing emotional facial expressions. Brain, 121, 47–57. Morris, J. S., Frith, C. D., Perrett, D. I., Rowland, D., Young, A. W., Calder, A. J., & Dolan, R. J. (1996). A differential neural response in the human amygdala to fearful and happy facial expressions. Nature, 383, 812–815. doi:10.1038/383812a0 Öhman, A., & Mineka, S. (2001). Fears, phobias, and preparedness: Toward an evolved module of fear and fear learning. Psychological Review, 108, 483–522. doi:10.1037/0033-295X.108.3.483 Pessoa, L., Japee, S., Sturman, D., & Ungerleider, L. G. (2006). Target visibility and visual awareness modulate amygdala responses to fearful faces. Cerebral Cortex, 16, 366–375. doi:10.1093/cercor/bhi115 Pessoa, L., Japee, S., & Ungerleider, L. G. (2005). Visual awareness and the detection of fearful faces. Emotion, 5, 243–247. doi:10.1037/1528-3542.5.2.243 Pessoa, L., McKenna, M., Gutierrez, E., & Ungerleider, L. G. (2002). Neural processing of emotional faces requires attention. Proceedings of the National Academy of Sciences, 99, 11458–11463. doi:10.1073/pnas.172403899 Phelps, E. A., Delgado, M. R., Nearing, K. I., & LeDoux, J. E. (2004). Extinction learning in humans: Role of the amygdala and vmPFC. Neuron, 43, 897–905. doi:10.1016/j.neuron.2004.08.042 Porrino, L. J., Crane, A. M., & Goldman-Rakic, P. S. (1981). Direct and indirect pathways from the amygdala to the frontal lobe in rhesus monkeys. Journal of Comparative Neurology, 198, 121–136. doi:10.1002/cne.901980111 Richards, A., French, C. C., Calder, A. J., Webb, B., Fox, R., & Young, A. W. (2002). Anxiety-related bias in the classification of emotionally ambiguous facial expressions. Emotion, 2, 273–287. Russchen, F. T., Bakst, I., Amaral, D. G., & Price, J. L. (1985). The amygdalostriatal projections in the monkey: An anterograde tracing study. Brain Research, 329, 241–257. Samejima, K., Ueda, Y., Doya, K., & Kimura, M. (2005). Representation of action-specific reward values in the striatum. Science, 310, 1337–1340. doi:10.1126/science.1115270 Schoenbaum, G., & Roesch, M. (2005). Orbitofrontal cortex, associative learning, and expectancies. Neuron, 47, 633–636. doi:10.1016/j.neuron.2005.07.018 Schultz, W., & Dickinson, A. (2000). Neuronal coding of prediction errors. Annual Review of Neuroscience, 23, 473–500. doi:10.1146/annurev.neuro.23.1.473 Spielberger, C. D. (1983). Manual for the State–Trait Anxiety Inventory (Form Y). Palo Alto: Consulting Psychologists Press. Stewart, M. E., Ebmeier, K. P., & Deary, I. J. (2005). Personality correlates of happiness and sadness: EPQ-R and TPQ compared. Personality and Individual Differences, 38, 1085–1096. doi:10.1016/j.paid.2004.07.007 Surcinelli, P., Codispoti, M., Montebarocci, O., Rossi, N., & Baldaro, B. (2006). Facial emotion recognition in trait anxiety. Journal of Anxiety Disorders, 20, 110–117. doi:10.1016/j.janxdis.2004.11.010 Talairach, J., & Tournoux, P. (1988). Co-planar stereotaxic atlas of the human brain: 3-D proportional system: An approach to cerebral imaging. New York: Thieme. Tobler, P. N., O’Doherty, J. P., Dolan, R. J., & Schultz, W. (2006). Human neural learning depends on reward prediction errors in the blocking paradigm. Journal of Neurophysiology, 95, 301–310. doi:10.1152/jn.00762.2005 Vogt, B. A., & Pandya, D. N. (1987). Cingulate cortex of the rhesus monkey: II. Cortical afferents. Journal of Comparative Neurology, 262, 271–289. doi:10.1002/cne.902620208 Whalen, P. J., Rauch, S. L., Etcoff, N. L., McInerney, S. C., Lee, M. B., & Jenike, M. A. (1998). Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge. Journal of Neuroscience, 18, 411–418. Wilson, E., & MacLeod, C. (2003). Contrasting two accounts of anxiety-linked attentional bias: Selective attention to varying levels of stimulus threat intensity. Journal of Abnormal Psychology, 112, 212–218. Winecoff, A., Clithero, J. A., Carter, R. M., Bergman, S. R., Wang, L., & Huettel, S. A. (2013). Ventromedial prefrontal cortex encodes emotional value. Journal of Neuroscience, 33, 11032–11039. doi:10.1523/JNEUROSCI.4317-12.2013 Winton, E. C., Clark, D. M., & Edelmann, R. J. (1995). Social anxiety, fear of negative evaluation and the detection of negative emotion in others. Behaviour Research and Therapy, 33, 193–196. Young, L., Bechara, A., Tranel, D., Damasio, H., Hauser, M., & Damasio, A. (2010). Damage to ventromedial prefrontal cortex impairs judgment of harmful intent. Neuron, 65, 845–851. doi:10.1016/j.neuron.2010.03.003