Assessing inter-individual differences with task-related functional neuroimaging

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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. 1.

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

  2. 2.

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

  3. 3.

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

  4. 4.

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

  5. 5.

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

  6. 6.

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

  7. 7.

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

  8. 8.

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

  9. 9.

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

  10. 10.

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

  11. 11.

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

  12. 12.

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

  13. 13.

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

  14. 14.

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

  15. 15.

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

  16. 16.

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

  17. 17.

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

  18. 18.

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

  19. 19.

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

  20. 20.

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

  21. 21.

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

  22. 22.

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

  23. 23.

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

  24. 24.

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

  25. 25.

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

  26. 26.

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

  27. 27.

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

  28. 28.

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

  29. 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. 30.

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

  31. 31.

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

  32. 32.

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

  33. 33.

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

  34. 34.

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

  35. 35.

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

  36. 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. 37.

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

  38. 38.

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

  39. 39.

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

  40. 40.

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

  41. 41.

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

  42. 42.

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

  43. 43.

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

  44. 44.

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

  45. 45.

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

  46. 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. 47.

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

  48. 48.

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

  49. 49.

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

  50. 50.

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

  51. 51.

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

  52. 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. 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. 54.

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

  55. 55.

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

  56. 56.

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

  57. 57.

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

  58. 58.

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

  59. 59.

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

  60. 60.

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

  61. 61.

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

  62. 62.

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

  63. 63.

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

  64. 64.

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

  65. 65.

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

  66. 66.

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

  67. 67.

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

  68. 68.

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

  69. 69.

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

  70. 70.

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

  71. 71.

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

  72. 72.

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

  73. 73.

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

  74. 74.

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

  75. 75.

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

  76. 76.

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

  77. 77.

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

  78. 78.

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

  79. 79.

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

  80. 80.

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

  81. 81.

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

  82. 82.

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

  83. 83.

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

  84. 84.

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

  85. 85.

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

  86. 86.

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

  87. 87.

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

  88. 88.

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

  89. 89.

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

  90. 90.

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

  91. 91.

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

  92. 92.

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

  93. 93.

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

  94. 94.

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

  95. 95.

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

  96. 96.

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

  97. 97.

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

  98. 98.

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

  99. 99.

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

  100. 100.

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

  101. 101.

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

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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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Correspondence to Maël Lebreton.

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