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Neural mechanisms underlying subsequent memory for personal beliefs:An fMRI study

  • Erik A. Wing
  • Vijeth Iyengar
  • Thomas M. Hess
  • Kevin S. LaBar
  • Scott A. Huettel
  • Roberto Cabeza
Article
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Abstract

Many fMRI studies have examined the neural mechanisms supporting emotional memory for stimuli that generate emotion rather automatically (e.g., a picture of a dangerous animal or of appetizing food). However, far fewer studies have examined how memory is influenced by emotion related to social and political issues (e.g., a proposal for large changes in taxation policy), which clearly vary across individuals. In order to investigate the neural substrates of affective and mnemonic processes associated with personal opinions, we employed an fMRI task wherein participants rated the intensity of agreement/disagreement to sociopolitical belief statements paired with neural face pictures. Following the rating phase, participants performed an associative recognition test in which they distinguished identical versus recombined face–statement pairs. The study yielded three main findings: behaviorally, the intensity of agreement ratings was linked to greater subjective emotional arousal as well as enhanced high-confidence subsequent memory. Neurally, statements that elicited strong (vs. weak) agreement or disagreement were associated with greater activation of the amygdala. Finally, a subsequent memory analysis showed that the behavioral memory advantage for statements generating stronger ratings was dependent on the medial prefrontal cortex (mPFC). Together, these results both underscore consistencies in neural systems supporting emotional arousal and suggest a modulation of arousal-related encoding mechanisms when emotion is contingent on referencing personal beliefs.

Keywords

Amygdala Emotion Episodic memory 
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Notes

Acknowledgements

This work was supported by a grant from the National Institutes on Aging (R01-AG34580-03) awarded to R.C. and a National Science Foundation (NSF) Graduate Research Fellowship (Grant Number 110640) awarded to V.I. We thank Alexandra Atkins for assistance with programming and piloting the paradigm, David Chou for assisting in data management and analysis, and Kerry Townsend for assisting in data collection.

References

  1. Adolphs, R., Russell, J. A., & Tranel, D. (1999). A role for the human amygdala in recognizing emotional arousal from unpleasant stimuli. Psychological Science, 10(2), 167–171.  https://doi.org/10.1111/1467-9280.00126 CrossRefGoogle Scholar
  2. Amodio, D. M., & Frith, C. D. (2006). Meeting of minds: The medial frontal cortex and social cognition. Nature Reviews Neuroscience, 7(4), 268–77.  https://doi.org/10.1038/nrn1884 CrossRefPubMedGoogle Scholar
  3. Benoit, R. G., Gilbert, S. J., Volle, E., & Burgess, P. W. (2010). When I think about me and simulate you: Medial rostral prefrontal cortex and self-referential processes. NeuroImage, 50(3), 1340–1349.  https://doi.org/10.1016/j.neuroimage.2009.12.091 CrossRefPubMedGoogle Scholar
  4. Bentley, S. V., Greenaway, K. H., & Haslam, S. A. (2017). An online paradigm for exploring the self-reference effect. PLOS ONE, 12(5), e0176611.  https://doi.org/10.1371/journal.pone.0176611 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bradley, S. D., Angelini, J. R., & Lee, S. (2007). Psychophysiological and memory effects of negative political ADS: Aversive, arousing, and well remembered. Journal of Advertising, 36(4), 115–127.  https://doi.org/10.2753/JOA0091-3367360409 CrossRefGoogle Scholar
  6. Brod, G., Lindenberger, U., Wagner, A. D., & Shing, Y. L. (2016). Knowledge acquisition during exam preparation improves memory and modulates memory formation. The Journal of Neuroscience, 36(31), 8103–8111.  https://doi.org/10.1523/JNEUROSCI.0045-16.2016 CrossRefPubMedGoogle Scholar
  7. Bruneau, E. G., & Saxe, R. (2010). Attitudes towards the outgroup are predicted by activity in the precuneus in Arabs and Israelis. NeuroImage, 52(4), 1704–1711.  https://doi.org/10.1016/j.neuroimage.2010.05.057 CrossRefPubMedGoogle Scholar
  8. Cahill, L., & McGaugh, J. (1995). A novel demonstration of enhanced memory associated with emotional arousal. Consciousness and Cognition, 4, 410–421.CrossRefPubMedGoogle Scholar
  9. Cahill, L., & McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends in Neurosciences, 21(7), 294–299.CrossRefPubMedGoogle Scholar
  10. Cassidy, B. S., Leshikar, E. D., Shih, J. Y., Aizenman, A., & Gutchess, A. H. (2013). Valence-based age differences in medial prefrontal activity during impression formation. Social Neuroscience, 8(5), 462–473.  https://doi.org/10.1080/17470919.2013.832373 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Civettini, A., & Redlawsk, D. (2009). Voters, emotions, and memory. Political Psychology, 30(1), 125–151.CrossRefGoogle Scholar
  12. D’Argembeau, A., Ruby, P., Collette, F., Degueldre, C., Balteau, E., Luxen, A., … Salmon, E. (2007). Distinct regions of the medial prefrontal cortex are associated with self-referential processing and perspective taking. Journal of Cognitive Neuroscience, 19(6), 935–944.  https://doi.org/10.1162/jocn.2007.19.6.935
  13. Denny, B. T., Kober, H., Wager, T. D., & Ochsner, K. N. (2012). A meta-analysis of functional neuroimaging studies of self- and other judgments reveals a spatial gradient for mentalizing in medial prefrontal cortex. Journal of Cognitive Neuroscience, 24(8), 1742–1752.  https://doi.org/10.1162/jocn_a_00233 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Diano, M., Celeghin, A., Bagnis, A., & Tamietto, M. (2017). Amygdala response to emotional stimuli without awareness: Facts and interpretations. Frontiers in Psychology, 7:2029.  https://doi.org/10.3389/fpsyg.2016.02029 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Dolcos, F., LaBar, K. S., & Cabeza, R. (2004a). Dissociable effects of arousal and valence on prefrontal activity indexing emotional evaluation and subsequent memory: An event-related fMRI study. NeuroImage, 23(1), 64–74.  https://doi.org/10.1016/j.neuroimage.2004.05.015 CrossRefPubMedGoogle Scholar
  16. Dolcos, F., LaBar, K. S., & Cabeza, R. (2004b). Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events. Neuron, 42(5), 855–863.CrossRefPubMedGoogle Scholar
  17. Dolcos, F., LaBar, K. S., & Cabeza, R. (2005). Remembering one year later: Role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proceedings of the National Academy of Sciences, 102(7), 2626–2631.  https://doi.org/10.1073/pnas.0409848102 CrossRefGoogle Scholar
  18. Dougal, S., Phelps, E. A., & Davachi, L. (2007). The role of medial temporal lobe in item recognition and source recollection of emotional stimuli. Cognitive, Affective & Behavioral Neuroscience, 7(3), 233–242.CrossRefGoogle Scholar
  19. Gilron, R., & Gutchess, A. H. (2012). Remembering first impressions: Effects of intentionality and diagnosticity on subsequent memory. Cognitive, Affective, & Behavioral Neuroscience, 12(1), 85–98.  https://doi.org/10.3758/s13415-011-0074-6 CrossRefGoogle Scholar
  20. Gozzi, M., Zamboni, G., Krueger, F., & Grafman, J. (2010). Interest in politics modulates neural activity in the amygdala and ventral striatum. Human Brain Mapping, 31(11), 1763–1771.  https://doi.org/10.1002/hbm.20976 PubMedGoogle Scholar
  21. Gutchess, A. H., Kensinger, E. A., & Schacter, D. L. (2010). Functional neuroimaging of self-referential encoding with age. Neuropsychologia, 48(1), 211–219. Retrieved from http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2794905&tool=pmcentrez&rendertype=abstract CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hamann, S. (2001). Cognitive and neural mechanisms of emotional memory. Trends in Cognitive Sciences, 5(9), 394–400.CrossRefPubMedGoogle Scholar
  23. Harris, S., Kaplan, J. T., Curiel, A., Bookheimer, S. Y., Iacoboni, M., & Cohen, M. S. (2009). The neural correlates of religious and nonreligious belief. PLOS ONE, 4(10), e7272  https://doi.org/10.1371/journal.pone.0007272 CrossRefPubMedCentralGoogle Scholar
  24. Harvey, P.-O., Fossati, P., & Lepage, M. (2007). Modulation of memory formation by stimulus content: Specific role of the medial prefrontal cortex in the successful encoding of social pictures. Journal of Cognitive Neuroscience, 19(2), 351–362.  https://doi.org/10.1162/jocn.2007.19.2.351 CrossRefPubMedGoogle Scholar
  25. Heatherton, T. F., Wyland, C. L., Macrae, C. N., Demos, K. E., Denny, B. T., & Kelley, W. M. (2006). Medial prefrontal activity differentiates self from close others. Social Cognitive and Affective Neuroscience, 1(1), 18–25.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kaplan, J. T., Freedman, J., & Iacoboni, M. (2007). Us versus them: Political attitudes and party affiliation influence neural response to faces of presidential candidates. Neuropsychologia, 45(1), 55–64.  https://doi.org/10.1016/j.neuropsychologia.2006.04.024 CrossRefPubMedGoogle Scholar
  27. Kelley, W. M., Macrae, C. N., Wyland, C. L., Caglar, S., Inati, S., & Heatherton, T. F. (2002). Finding the self? An event-related fMRI study. Journal of Cognitive Neuroscience, 14(5), 785–794.  https://doi.org/10.1162/08989290260138672 CrossRefPubMedGoogle Scholar
  28. Kensinger, E. A., & Schacter, D. L. (2006). Amygdala activity is associated with the successful encoding of item, but not source, information for positive and negative stimuli. The Journal of Neuroscience, 26(9), 2564–70.  https://doi.org/10.1523/JNEUROSCI.5241-05.2006 CrossRefPubMedGoogle Scholar
  29. Kim, H. (2011). Neural activity that predicts subsequent memory and forgetting: A meta-analysis of 74 fMRI studies. NeuroImage, 54(3), 2446–2461.  https://doi.org/10.1016/j.neuroimage.2010.09.045 CrossRefPubMedGoogle Scholar
  30. Knutson, K. M., Wood, J. N., Spampinato, M. V, & Grafman, J. (2006). Politics on the brain: An FMRI investigation. Social Neuroscience, 1(1), 25–40.  https://doi.org/10.1080/17470910600670603 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Konkel, A., & Cohen, N. J. (2009). Relational memory and the hippocampus: Representations and methods. Frontiers in Neuroscience, 3(2), 166–174.  https://doi.org/10.3389/neuro.01.023.2009 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Kumaran, D., & Maguire, E. A. (2009). Novelty signals: A window into hippocampal information processing. Trends in Cognitive Sciences, 13(2), 47–54.  https://doi.org/10.1016/j.tics.2008.11.004 CrossRefPubMedGoogle Scholar
  33. LaBar, K. S., & Cabeza, R. (2006). Cognitive neuroscience of emotional memory. Nature Reviews Neuroscience, 7(1), 54–64.  https://doi.org/10.1038/nrn1825 CrossRefPubMedGoogle Scholar
  34. Lang, P. J., Bradley, M. M., & Cuthbert, B. N. (1997). International affective picture system (IAPS): Technical manual and affective ratings Gainesville: NIMH Center for the Study of Emotion and Attention.Google Scholar
  35. Leshikar, E. D., Cassidy, B. S., & Gutchess, A. H. (2016). Similarity to the self influences cortical recruitment during impression formation. Cognitive, Affective, & Behavioral Neuroscience, 16, 302–314.  https://doi.org/10.3758/s13415-015-0390-3 CrossRefGoogle Scholar
  36. Leshikar, E. D., & Duarte, A. (2012). Medial prefrontal cortex supports source memory accuracy for self-referenced items. Social Neuroscience, 7(2), 126–145.  https://doi.org/10.1080/17470919.2011.585242 CrossRefPubMedGoogle Scholar
  37. Macrae, C. N., Moran, J. M., Heatherton, T. F., Banfield, J. F., & Kelley, W. M. (2004). Medial prefrontal activity predicts memory for self. Cerebral Cortex, 14(6), 647–654.  https://doi.org/10.1093/cercor/bhh025 CrossRefPubMedGoogle Scholar
  38. Mather, M. (2007). Emotional arousal and memory binding: An object-based framework. Perspectives on Psychological Science, 2(1), 33–52.CrossRefPubMedGoogle Scholar
  39. Minear M, Park DC (2004) A lifespan database of adult facial stimuli. Behavior Research Methods, Instruments, & Computers 36(4):630–633Google Scholar
  40. Mitchell, J. P., Banaji, M. R., & Macrae, C. N. (2005). The link between social cognition and self-referential thought in the medial prefrontal cortex. Journal of Cognitive Neuroscience, 17(8), 1306–15.  https://doi.org/10.1162/0898929055002418 CrossRefPubMedGoogle Scholar
  41. Mitchell, J. P., Macrae, C. N., & Banaji, M. R. (2004). Encoding-specific effects of social cognition on the neural correlates of subsequent memory. The Journal of Neuroscience, 24(21), 4912–4917.  https://doi.org/10.1523/JNEUROSCI.0481-04.2004 CrossRefPubMedGoogle Scholar
  42. Mitchell, J. P., Macrae, C. N., & Banaji, M. R. (2006). Dissociable medial prefrontal contributions to judgments of similar and dissimilar others. Neuron, 50(4), 655–663.  https://doi.org/10.1016/j.neuron.2006.03.040 CrossRefPubMedGoogle Scholar
  43. Northoff, G., Heinzel, A., de Greck, M., Bermpohl, F., Dobrowolny, H., & Panksepp, J. (2006). Self-referential processing in our brain—A meta-analysis of imaging studies on the self. NeuroImage, 31(1), 440–57.  https://doi.org/10.1016/j.neuroimage.2005.12.002 CrossRefPubMedGoogle Scholar
  44. Pais-Vieira, C., Wing, E. A., & Cabeza, R. (2016). The influence of self-awareness on emotional memory formation: An fMRI study. Social Cognitive and Affective Neuroscience, 11(4), 580–592.  https://doi.org/10.1093/scan/nsv141 CrossRefPubMedGoogle Scholar
  45. Paller, K. A., & Wagner, A. D. (2002). Observing the transformation of experience into memory. Trends in Cognitive Sciences, 6(2), 93–102.CrossRefPubMedGoogle Scholar
  46. Phan, K. L., Wager, T., Taylor, S. F., & Liberzon, I. (2002). Functional neuroanatomy of emotion: A meta-analysis of emotion activation studies in PET and fMRI. NeuroImage, 16(2), 331–348.  https://doi.org/10.1006/nimg.2002.1087 CrossRefPubMedGoogle Scholar
  47. Phelps, E. A., & LeDoux, J. E. (2005). Contributions of the amygdala to emotion processing: From animal models to human behavior. Neuron, 48(2), 175–187.  https://doi.org/10.1016/j.neuron.2005.09.025 CrossRefPubMedGoogle Scholar
  48. Quamme, J. R., Yonelinas, A. P., & Norman, K. A. (2007). Effect of unitization on associative recognition in amnesia. Hippocampus, 200, 192–200.  https://doi.org/10.1002/hipo CrossRefGoogle Scholar
  49. Ritchey, M., LaBar, K. S., & Cabeza, R. (2011). Level of processing modulates the neural correlates of emotional memory formation. Journal of Cognitive Neuroscience, 23(4), 757–771.  https://doi.org/10.1162/jocn.2010.21487 CrossRefPubMedGoogle Scholar
  50. Said, C. P., Baron, S. G., & Todorov, A. (2009). Nonlinear amygdala response to face trustworthiness: Contributions of high and low spatial frequency information. Journal of Cognitive Neuroscience, 21(3), 519–528.  https://doi.org/10.1162/jocn.2009.21041 CrossRefPubMedGoogle Scholar
  51. Said, C. P., Dotsch, R., & Todorov, A. (2010). The amygdala and FFA track both social and non-social face dimensions. Neuropsychologia, 48(12), 3596–605.  https://doi.org/10.1016/j.neuropsychologia.2010.08.009 CrossRefPubMedGoogle Scholar
  52. Sakaki, M., Niki, K., & Mather, M. (2012). Beyond arousal and valence: The importance of the biological versus social relevance of emotional stimuli. Cognitive, Affective, & Behavioral Neuroscience, 12(1), 115–39.  https://doi.org/10.3758/s13415-011-0062-x CrossRefGoogle Scholar
  53. Santos, A., Mier, D., Kirsch, P., & Meyer-Lindenberg, A. (2011). Evidence for a general face salience signal in human amygdala. NeuroImage, 54(4), 3111–3116.  https://doi.org/10.1016/j.neuroimage.2010.11.024 CrossRefPubMedGoogle Scholar
  54. Small, D. M., Gregory, M. D., Mak, Y. E., Gitelman, D., Mesulam, M. M., & Parrish, T. (2003). Dissociation of neural representation of intensity and affective valuation in human gustation. Neuron, 39(4), 701–711. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/12925283 CrossRefPubMedGoogle Scholar
  55. Snodgrass, J. G., & Corwin, J. (1988). Pragmatics of measuring recognition memory: Applications to dementia and amnesia. Journal of Experimental Psychology: General, 117(1), 34–50.CrossRefGoogle Scholar
  56. Spaniol, J., Davidson, P. S. R., Kim, A. S. N., Han, H., Moscovitch, M., & Grady, C. L. (2009). Event-related fMRI studies of episodic encoding and retrieval: Meta-analyses using activation likelihood estimation. Neuropsychologia, 47(8/9), 1765–1779.  https://doi.org/10.1016/j.neuropsychologia.2009.02.028 CrossRefPubMedGoogle Scholar
  57. Symons, C. S., & Johnson, B. T. (1997). The self-reference effect in memory: A meta-analysis. Psychological Bulletin, 121(3), 371–394.  https://doi.org/10.1037/0033-2909.121.3.371 CrossRefPubMedGoogle Scholar
  58. Talmi, D., Anderson, A. K., Riggs, L., Caplan, J. B., & Moscovitch, M. (2008). Immediate memory consequences of the effect of emotion on attention to pictures. Learning & Memory (Cold Spring Harbor, N.Y.), 15(3), 172–82.  https://doi.org/10.1101/lm.722908 CrossRefGoogle Scholar
  59. Tse, D., Langston, R. F., Kakeyama, M., Bethus, I., Spooner, P. A., Wood, E. R., … Morris, R. G. M. (2007). Schemas and memory consolidation. Science, 316(5821), 76–82.  https://doi.org/10.1126/science.1135935
  60. Tse, D., Takeuchi, T., Kakeyama, M., Kajii, Y., Okuno, H., Tohyama, C., … Morris, R. G. M. (2011). Schema-dependent gene activation and memory encoding in neocortex. Science, 333(6044), 891–895.  https://doi.org/10.1126/science.1205274
  61. Tsukiura, T., & Cabeza, R. (2011). Remembering beauty: Roles of orbitofrontal and hippocampal regions in successful memory encoding of attractive faces. NeuroImage, 54(1), 653–660.  https://doi.org/10.1016/j.neuroimage.2010.07.046 CrossRefPubMedGoogle Scholar
  62. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., … Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.  https://doi.org/10.1006/nimg.2001.0978
  63. van Kesteren, M. T. R., Beul, S. F., Takashima, A., Henson, R. N., Ruiter, D. J., & Fernández, G. (2013). Differential roles for medial prefrontal and medial temporal cortices in schema-dependent encoding: From congruent to incongruent. Neuropsychologia, 51(12), 2352–2359.  https://doi.org/10.1016/j.neuropsychologia.2013.05.027 CrossRefPubMedGoogle Scholar
  64. van Kesteren, M. T. R., Rijpkema, M., Ruiter, D. J., & Fernández, G. (2010). Retrieval of associative information congruent with prior knowledge is related to increased medial prefrontal activity and connectivity. The Journal of Neuroscience, 30(47), 15888–15894.  https://doi.org/10.1523/JNEUROSCI.2674-10.2010 CrossRefPubMedGoogle Scholar
  65. van Kesteren, M. T. R., Ruiter, D. J., Fernández, G., & Henson, R. N. (2012). How schema and novelty augment memory formation. Trends in Neurosciences, 35(4), 211–219.  https://doi.org/10.1016/j.tins.2012.02.001 CrossRefPubMedGoogle Scholar
  66. Wagner, D. D., Haxby, J. V., & Heatherton, T. F. (2012). The representation of self and person knowledge in the medial prefrontal cortex. WIREs Cognitive Science, 3(4), 451–470.  https://doi.org/10.1002/wcs.1183 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Ward, B. D. (2000). Simultaneous inference for fMRI data. Milwaukee: AFNI 3dDeconvolve Documentation, Medical College of Wisconsin.Google Scholar
  68. Winston, J. S., O’Doherty, J., Kilner, J. M., Perrett, D. I., & Dolan, R. J. (2007). Brain systems for assessing facial attractiveness. Neuropsychologia, 45(1), 195–206.  https://doi.org/10.1016/j.neuropsychologia.2006.05.009 CrossRefPubMedGoogle Scholar
  69. Zald, D. H. (2003). The human amygdala and the emotional evaluation of sensory stimuli. Brain Research Reviews, 41(1), 88–123.CrossRefPubMedGoogle Scholar
  70. Zamboni, G., Gozzi, M., Krueger, F., Duhamel, J.-R., Sirigu, A., & Grafman, J. (2009). Individualism, conservatism, and radicalism as criteria for processing political beliefs: A parametric fMRI study. Social Neuroscience, 4(5), 367–383.  https://doi.org/10.1080/17470910902860308 CrossRefPubMedGoogle Scholar

Copyright information

© Psychonomic Society, Inc. 2018

Authors and Affiliations

  • Erik A. Wing
    • 1
  • Vijeth Iyengar
    • 1
  • Thomas M. Hess
    • 2
  • Kevin S. LaBar
    • 1
  • Scott A. Huettel
    • 1
  • Roberto Cabeza
    • 1
  1. 1.Center for Cognitive NeuroscienceDuke UniversityDurhamUSA
  2. 2.Department of PsychologyNorth Carolina State UniversityRaleighUSA

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