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Assessing inter-individual differences with task-related functional neuroimaging

Abstract

Explaining and predicting individual behavioural differences induced by clinical and social factors constitutes one of the most promising applications of neuroimaging. In this Perspective, we discuss the theoretical and statistical foundations of the analyses of inter-individual differences in task-related functional neuroimaging. Leveraging a five-year literature review (July 2013–2018), we show that researchers often assess how activations elicited by a variable of interest differ between individuals. We argue that the rationale for such analyses, typically grounded in resource theory, offers an over-large analytical and interpretational flexibility that undermines their validity. We also recall how, in the established framework of the general linear model, inter-individual differences in behaviour can act as hidden moderators and spuriously induce differences in activations. We conclude with a set of recommendations and directions, which we hope will contribute to improving the statistical validity and the neurobiological interpretability of inter-individual difference analyses in task-related functional neuroimaging.

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Fig. 1: A case study: explaining inter-individual differences in learning with model-based fMRI.
Fig. 2: From differences in behaviour to IBBD.

References

  1. Cronbach, L. J. Am. Psychol. 12, 671–684 (1957).

    Google Scholar 

  2. Underwood, B. J. Am. Psychol. 30, 128–134 (1975).

    Google Scholar 

  3. Vogel, E. K. & Awh, E. Curr. Dir. Psychol. Sci. 17, 171–176 (2008).

    Google Scholar 

  4. Van Horn, J. D., Grafton, S. T. & Miller, M. B. Brain Imaging Behav. 2, 327–334 (2008).

    PubMed  PubMed Central  Google Scholar 

  5. Dubois, J. & Adolphs, R. Trends Cogn. Sci. 20, 425–443 (2016).

    PubMed  PubMed Central  Google Scholar 

  6. Braver, T. S., Cole, M. W. & Yarkoni, T. Curr. Opin. Neurobiol. 20, 242–250 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. McGonigle, D. J. Neuroimage 62, 1116–1120 (2012).

    PubMed  Google Scholar 

  8. Gabrieli, J. D. E., Ghosh, S. S. & Whitfield-Gabrieli, S. Neuron 85, 11–26 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Seghier, M. L. & Price, C. J. Trends Cogn. Sci. 22, 517–530 (2018).

    PubMed  PubMed Central  Google Scholar 

  10. Falk, E. B. et al. Proc. Natl. Acad. Sci. USA 110, 17615–17622 (2013).

    CAS  PubMed  Google Scholar 

  11. Luna, B., Padmanabhan, A. & O’Hearn, K. Brain Cogn. 72, 101–113 (2010).

    PubMed  Google Scholar 

  12. Barulli, D. & Stern, Y. Trends Cogn. Sci. 17, 502–509 (2013).

    PubMed  Google Scholar 

  13. Gregory, S., Long, J. D., Tabrizi, S. J. & Rees, G. Curr. Opin. Neurol. 30, 380–387 (2017).

    PubMed  PubMed Central  Google Scholar 

  14. Commins, S. Rev. Neurosci. 29, 183–197 (2017).

    Google Scholar 

  15. Matthews, P. M., Honey, G. D. & Bullmore, E. T. Nat. Rev. Neurosci. 7, 732–744 (2006).

    CAS  PubMed  Google Scholar 

  16. Kishida, K. T., King-Casas, B. & Montague, P. R. Neuron 67, 543–554 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Dagher, A. Neuroimage 151, 128–129 (2017).

    PubMed  Google Scholar 

  18. Camerer, C. F. Econ. J. 117, C26–C42 (2007).

    Google Scholar 

  19. Fehr, E. & Camerer, C. F. Trends Cogn. Sci. 11, 419–427 (2007).

    PubMed  Google Scholar 

  20. Rustichini, A. Curr. Opin. Neurobiol. 19, 672–677 (2009).

    CAS  PubMed  Google Scholar 

  21. Kable, J. W. & Levy, I. Curr. Opin. Behav. Sci. 5, 100–107 (2015).

    PubMed  PubMed Central  Google Scholar 

  22. Katsnelson, A. Proc. Natl. Acad. Sci. USA 112, 15530–15532 (2015).

    CAS  PubMed  Google Scholar 

  23. Kanai, R. & Rees, G. Nat. Rev. Neurosci. 12, 231–242 (2011).

    CAS  PubMed  Google Scholar 

  24. Wang, X.-J. & Krystal, J. H. Neuron 84, 638–654 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. O’Doherty, J. P., Hampton, A. & Kim, H. Ann. NY Acad. Sci. 1104, 35–53 (2007).

    PubMed  Google Scholar 

  26. Gläscher, J. P. & O’Doherty, J. P. Wiley Interdiscip. Rev. Cogn. Sci. 1, 501–510 (2010).

    PubMed  Google Scholar 

  27. Cohen, J. D. et al. Nat. Neurosci. 20, 304–313 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Patzelt, E. H., Hartley, C. A. & Gershman, S. J. Personal. Neurosci. 1, e18 (2018).

    Google Scholar 

  29. Daw, N.D. in Decision Making, Affect, and Learning: Attention and Performance XXIII (eds. Delgado, M.R., Phelps, E.A. & Robbins, T.W.) Chapter 1 (2011).

  30. Corrado, G. & Doya, K. J. Neurosci. 27, 8178–8180 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Chen, X., Holland, P. & Galea, J. M. Curr. Opin. Behav. Sci. 20, 83–88 (2018).

    Google Scholar 

  32. Joiner, J., Piva, M., Turrin, C. & Chang, S. W. C. NPJ Sci. Learn. 2, 8 (2017).

    PubMed  PubMed Central  Google Scholar 

  33. Dayan, P. & Daw, N. D. Cogn. Affect. Behav. Neurosci. 8, 429–453 (2008).

    PubMed  Google Scholar 

  34. Maia, T. V. & Frank, M. J. Nat. Neurosci. 14, 154–162 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Palminteri, S. & Pessiglione, M. in Decision Neuroscience (eds. Dreher, J.-C. & Tremblay, L.) 291–303 (Academic Press, 2017).

  36. Rescorla, R.A. & Wagner, A.R. in Classical Conditioning II: Current Research and Theory (eds. Black, A.H. & Prokasy, W.F.) 64–99 (Appleton-Century-Crofts, 1972).

  37. Sutton, R.S. & Barto, A.G. Reinforcement Learning: An Introduction. (Cambridge University Press, 1998).

  38. Garrison, J., Erdeniz, B. & Done, J. Neurosci. Biobehav. Rev. 37, 1297–1310 (2013).

    PubMed  Google Scholar 

  39. O’Doherty, J. et al. Science 304, 452–454 (2004).

    PubMed  Google Scholar 

  40. Daw, N. D., O’Doherty, J. P., Dayan, P., Seymour, B. & Dolan, R. J. Nature 441, 876–879 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J. & Frith, C. D. Nature 442, 1042–1045 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Montague, P. R., Dolan, R. J., Friston, K. J. & Dayan, P. Trends Cogn. Sci. 16, 72–80 (2012).

    PubMed  Google Scholar 

  43. Robinson, O. J. & Chase, H. W. Comput. Psychiatr. 1, 208–233 (2017).

    PubMed  PubMed Central  Google Scholar 

  44. Huys, Q. J. M., Maia, T. V. & Frank, M. J. Nat. Neurosci. 19, 404–413 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Stephan, K. E. et al. Neuroimage 145 Pt B, 180–199 (2017).

    Google Scholar 

  46. Harvey, A., Watkins, E., Mansell, W. & Shafran, R. Cognitive Behavioural Processes Across Psychological Disorders: A Transdiagnostic Approach to Research and Treatment. (Oxford University Press, 2004).

  47. Poldrack, R. A. Dev. Cogn. Neurosci. 11, 12–17 (2015).

    PubMed  Google Scholar 

  48. Norman, D. A. & Bobrow, D. G. Cogn. Psychol. 7, 44–64 (1975).

    Google Scholar 

  49. Navon, D. & Gopher, D. Psychol. Rev. 86, 214–255 (1979).

    Google Scholar 

  50. Humphreys, M. S. & Revelle, W. Psychol. Rev. 91, 153–184 (1984).

    CAS  PubMed  Google Scholar 

  51. Navon, D. Psychol. Rev. 91, 216–234 (1984).

    Google Scholar 

  52. Matthews, G., Warm, J.S., Reinerman, L.E., Langheim, L.K. & Saxby, D.J. in Handbook of Individual Differences in Cognition: Attention, Memory, and Executive Control (eds. Gruszka, A., Matthews, G. & Szymura, B.) 205–230 (Springer New York, 2010).

  53. Yarkoni, T. & Braver, T.S. in Handbook of Individual Differences in Cognition (eds. Gruszka, A., Matthews, G. & Szymura, B.) 87–107 (Springer New York, 2010).

  54. Cox, K. M. & Kable, J. W. J. Neurosci. 34, 16533–16543 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Louie, K. & Glimcher, P. W. Ann. NY Acad. Sci. 1251, 13–32 (2012).

    PubMed  Google Scholar 

  56. Padoa-Schioppa, C. J. Neurosci. 29, 14004–14014 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Rangel, A. & Clithero, J. A. Curr. Opin. Neurobiol. 22, 970–981 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Kerr, N. L. Soc. Psychol. 2, 196–217 (1998).

    CAS  Google Scholar 

  59. Nuzzo, R. Nature 526, 182–185 (2015).

    CAS  PubMed  Google Scholar 

  60. Munafò, M. R. et al. Nat. Hum. Behav. https://doi.org/10.1038/s41562-016-0021 (2017).

  61. Poldrack, R. A. et al. Nat. Rev. Neurosci. 18, 115–126 (2017).

    CAS  PubMed  Google Scholar 

  62. Hajcak, G., Meyer, A. & Kotov, R. J. Abnorm. Psychol. 126, 823–834 (2017).

    PubMed  Google Scholar 

  63. Hedge, C., Powell, G. & Sumner, P. Behav. Res. Methods https://doi.org/10.3758/s13428-017-0935-1 (2018).

    PubMed Central  Google Scholar 

  64. Pedroni, A. et al. Nat. Hum. Behav. 1, 803–809 (2017).

    PubMed  Google Scholar 

  65. Button, K. S. et al. Nat. Rev. Neurosci. 14, 365–376 (2013).

    CAS  PubMed  Google Scholar 

  66. Szucs, D. & Ioannidis, J. P. A. PLoS Biol. 15, e2000797 (2017).

    PubMed  PubMed Central  Google Scholar 

  67. Abi-Dargham, A. & Horga, G. Nat. Med. 22, nm.4190 (2016).

    Google Scholar 

  68. Caceres, A., Hall, D. L., Zelaya, F. O., Williams, S. C. R. & Mehta, M. A. Neuroimage 45, 758–768 (2009).

    PubMed  Google Scholar 

  69. Plichta, M. M. et al. Neuroimage 60, 1746–1758 (2012).

    PubMed  Google Scholar 

  70. Nord, C. L., Gray, A., Charpentier, C. J., Robinson, O. J. & Roiser, J. P. Neuroimage 156, 119–127 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Renvall, V., Nangini, C. & Hari, R. Sci. Rep. 4, 3920 (2014).

    PubMed  PubMed Central  Google Scholar 

  72. Mueller, S. et al. Neuron 77, 586–595 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  73. Laumann, T. O. et al. Neuron 87, 657–670 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Honey, G. & Bullmore, E. Trends Pharmacol. Sci. 25, 366–374 (2004).

    CAS  PubMed  Google Scholar 

  75. Bestmann, S. & Feredoes, E. Ann. NY Acad. Sci. 1296, 11–30 (2013).

    PubMed  Google Scholar 

  76. Polanía, R., Nitsche, M. A. & Ruff, C. C. Nat. Neurosci. 21, 174–187 (2018).

    PubMed  Google Scholar 

  77. Poldrack, R. A. & Gorgolewski, K. J. Nat. Neurosci. 17, 1510–1517 (2014).

    CAS  PubMed  Google Scholar 

  78. Barch, D. M. et al. Neuroimage 80, 169–189 (2013).

    PubMed  PubMed Central  Google Scholar 

  79. Miller, K. L. et al. Nat. Neurosci. 19, 1523–1536 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Van Essen, D. C. et al. Neuroimage 80, 62–79 (2013).

    PubMed  PubMed Central  Google Scholar 

  81. Wilson, R. C. & Niv, Y. PLOS Comput. Biol. 11, e1004237 (2015).

    PubMed  PubMed Central  Google Scholar 

  82. Cooper, S. R., Jackson, J. J., Barch, D. M. & Braver, T. S. Neurosci. Biobehav. Rev. 98, 29–46 (2019).

    PubMed  Google Scholar 

  83. Friston, K. Annu. Rev. Neurosci. 25, 221–250 (2002).

    CAS  PubMed  Google Scholar 

  84. Hunt, L. T. & Hayden, B. Y. Nat. Rev. Neurosci. 18, 172–182 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Silver, R. A. Nat. Rev. Neurosci. 11, 474–489 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Heeger, D. J. & Ress, D. Nat. Rev. Neurosci. 3, 142–151 (2002).

    CAS  PubMed  Google Scholar 

  87. Logothetis, N. K. Nature 453, 869–878 (2008).

    CAS  PubMed  Google Scholar 

  88. Gordon, E. M. et al. Neuron 95, 791–807.e7 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  89. Turk-Browne, N. B. Science 342, 580–584 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Bearden, C. E. & Thompson, P. M. Neuron 94, 232–236 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  91. Smith, S. M. & Nichols, T. E. Neuron 97, 263–268 (2018).

    CAS  PubMed  Google Scholar 

  92. Insel, T. R. & Cuthbert, B. N. Science 348, 499–500 (2015).

    CAS  PubMed  Google Scholar 

  93. Woo, C.-W., Chang, L. J., Lindquist, M. A. & Wager, T. D. Nat. Neurosci. 20, 365–377 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Hariri, A. R. Annu. Rev. Neurosci. 32, 225–247 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Congdon, E., Poldrack, R. A. & Freimer, N. B. Neuron 68, 218–230 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Gershman, S. J., Pesaran, B. & Daw, N. D. J. Neurosci. 29, 13524–13531 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Gläscher, J., Hampton, A. N. & O’Doherty, J. P. Cereb. Cortex 19, 483–495 (2009).

    PubMed  Google Scholar 

  98. Gläscher, J., Daw, N., Dayan, P. & O’Doherty, J. P. Neuron 66, 585–595 (2010).

    PubMed  PubMed Central  Google Scholar 

  99. Palminteri, S., Boraud, T., Lafargue, G., Dubois, B. & Pessiglione, M. J. Neurosci. 29, 13465–13472 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Palminteri, S., Khamassi, M., Joffily, M. & Coricelli, G. Nat. Commun. 6, 8096 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Pessiglione, M. et al. Neuron 59, 561–567 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

During the preparation of this work, M.L. was supported by a NWO Veni (Grant 451-15-015) and a Swiss National Found Ambizione grant (PZ00P3_174127). M.L. also acknowledges the support of the Bettencourt-Schueller Foundation. S.P. is supported by an ATIP-Avenir grant (R16069JS), the Programme Emergence(s) de la Ville de Paris, the Fyssen foundation, and the Fondation Schlumberger pour l’Education et la Recherche. The Institut d’Etude de la Cognition is supported financially by the LabEx IEC (ANR-10-LABX-0087 IEC) and the IDEX PSL* (ANR-10-IDEX-0001-02 PSL*).

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Lebreton, M., Bavard, S., Daunizeau, J. et al. Assessing inter-individual differences with task-related functional neuroimaging. Nat Hum Behav 3, 897–905 (2019). https://doi.org/10.1038/s41562-019-0681-8

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