Abstract
One foundational distinction in affective science is between emotion reactivity and regulation. This conceptual distinction has long been assumed to be instantiated in spatially separable brain systems (a typical example: amygdala/insula for reactivity and frontoparietal areas for regulation). In this research, we begin by reviewing previous findings that support and contradict the neural separability hypothesis concerning emotional reactivity and regulation. Further, we conduct a direct test of this hypothesis with empirical data. In five studies involving healthy and clinical samples (total n = 336), we assessed neural responses using fMRI while participants were asked to either react naturally or regulate their emotions (using reappraisal) while viewing emotionally evocative stimuli. Across five studies, we failed to find support for the neural separability hypothesis. In univariate analyses, both presumptive “reactivity” and “regulation” brain regions demonstrated equal or greater activation for the reactivity contrast than for the regulation contrast. In multivariate pattern analyses (MVPA), classifiers decoded reactivity (vs. neutral) trials more accurately than regulation (vs. reactivity) trials using multivoxel data in both presumptive “reactivity” and “regulation” regions. These findings suggest that emotion reactivity and regulation—as measured via fMRI—may not be as spatially separable in the brain as previously assumed. Our secondary whole-brain analyses revealed largely consistent results. We discuss the two theoretical possibilities regarding the neural separability hypothesis and offer thoughts for future research.
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Notes
Although the neural separability hypothesis would predict decreased activation in “reactivity” regions during down-regulation which can be useful information to perform the regulation classification above chance, its performance should still be lower than the performance for the reactivity classification.
References
Adolphs, R. (2010). What does the amygdala contribute to social cognition? Annals of the New York Academy of Sciences, 1191, 42–61. https://doi.org/10.1111/J.1749-6632.2010.05445.X
Averbeck, B. B., & Costa, V. D. (2017). Motivational neural circuits underlying reinforcement learning. Nature Neuroscience, 20(4), 505–512. https://doi.org/10.1038/nn.4506
Barrett, L. F. (2017). The theory of constructed emotion: An active inference account of interoception and categorization. Social Cognitive and Affective Neuroscience, 12(1), 1–23.
Barrett, L. F. (2013). Psychological construction: The darwinian approach to the science of emotion. Emotion Review, 5(4), 379–389. https://doi.org/10.1177/1754073913489753
Barrett, L. F., Mesquita, B., Ochsner, K. N., & Gross, J. J. (2007). The experience of emotion. Annual Review of Psychology, 58, 373–403. https://doi.org/10.1146/annurev.psych.58.110405.085709
Bo, K., Kraynak, T. E., Kwon, M., Sun, M., Gianaros, P. J., & Wager, T. D. (2023). Deconstructing the brain bases of emotion regulation: A systems-identification approach using Bayes factors (p. 2023.04.26.538485). bioRxiv. https://doi.org/10.1101/2023.04.26.538485
Buhle, J. T., Silvers, J. A., Wage, T. D., Lopez, R., Onyemekwu, C., Kober, H., Webe, J., & Ochsner, K. N. (2014). Cognitive reappraisal of emotion: A meta-analysis of human neuroimaging studies. Cerebral Cortex, 24(11), 2981–2990. https://doi.org/10.1093/cercor/bht154
Chang, L. J., Yarkoni, T., Khaw, M. W., & Sanfey, A. G. (2013). Decoding the role of the insula in human cognition: Functional parcellation and large-scale reverse inference. Cerebral Cortex, 23(3), 739–749. https://doi.org/10.1093/CERCOR/BHS065
Chang, L. J., Gianaros, P. J., Manuck, S. B., Krishnan, A., & Wager, T. D. (2015). A sensitive and specific neural signature for picture-induced negative affect. PLOS Biology, 13(6), e1002180. https://doi.org/10.1371/journal.pbio.1002180
Clark-Polner, E., Wager, T. D., Satpute, A. B., & Barrett, L. F. (2016). Neural fingerprinting: Meta-analysis, variation, and the search for brain-based essences in the science of emotion. In The handbook of emotion (4th ed., pp. 146–165). Guilford.
Denny, B. T., Inhoff, M. C., Zerubavel, N., Davachi, L., & Ochsner, K. N. (2015). Getting over it: Long-lasting effects of emotion regulation on amygdala response. Psychological Science, 26(9), 1377–1388. https://doi.org/10.1177/0956797615578863
Dixon, M. L., & Dweck, C. S. (2021). The amygdala and the prefrontal cortex: The co-construction of intelligent decision-making. Psychological Review, 129(6), 1414.
Dixon, M. L., Moodie, C. A., Goldin, P. R., Farb, N., Heimberg, R. G., & Gross, J. J. (2020). Emotion regulation in social anxiety disorder: Reappraisal and acceptance of negative self-beliefs. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 5(1), 119–129. https://doi.org/10.1016/j.bpsc.2019.07.009
Dixon, M. L., Moodie, C. A., Goldin, P. R., Farb, N., Heimberg, R. G., Zhang, J., & Gross, J. J. (2022). Frontoparietal and default mode network contributions to self-referential processing in social anxiety disorder. Cognitive, Affective and Behavioral Neuroscience, 22(1), 187–198.
Dosenbach, N. U. F., Fair, D. A., Miezin, F. M., Cohen, A. L., Wenger, K. K., Dosenbach, R. A. T., Fox, M. D., Snyder, A. Z., Vincent, J. L., Raichle, M. E., Schlaggar, B. L., & Petersen, S. E. (2007). Distinct brain networks for adaptive and stable task control in humans. Proceedings of the National Academy of Sciences of the United States of America, 104(26), 11073–11078. https://doi.org/10.1073/pnas.0704320104
Egner, T., Etkin, A., Gale, S., & Hirsch, J. (2008). Dissociable neural systems resolve conflict from emotional versus nonemotional distracters. Cerebral Cortex, 18(6), 1475–1484. https://doi.org/10.1093/CERCOR/BHM179
Etkin, A., Egner, T., Peraza, D. M., Kandel, E. R., & Hirsch, J. (2006). Resolving emotional conflict: A role for the rostral anterior cingulate cortex in modulating activity in the amygdala. Neuron, 51(6), 871–882. https://doi.org/10.1016/J.NEURON.2006.07.029
Etkin, A., Büchel, C., & Gross, J. J. (2015). The neural bases of emotion regulation. Nature Reviews Neuroscience, 16(11), 693–700. https://doi.org/10.1038/nrn4044
Frank, D. W., Dewitt, M., Hudgens-Haney, M., Schaeffer, D. J., Ball, B. H., Schwarz, N. F., Hussein, A. A., Smart, L. M., & Sabatinelli, D. (2014). Emotion regulation: Quantitative meta-analysis of functional activation and deactivation. Neuroscience and Biobehavioral Reviews, 45, 202–211. https://doi.org/10.1016/j.neubiorev.2014.06.010
Goldin, P. R., McRae, K., Ramel, W., & Gross, J. J. (2008). The neural bases of emotion regulation: Reappraisal and suppression of negative emotion. Biological Psychiatry, 63(6), 577–586. https://doi.org/10.1016/J.BIOPSYCH.2007.05.031
Goldin, P. R., Moodie, C. A., & Gross, J. J. (2019). Acceptance versus reappraisal: Behavioral, autonomic, and neural effects. Cognitive, Affective, & Behavioral Neuroscience, 19(4), 927–944. https://doi.org/10.3758/s13415-019-00690-7
Goldin, P. R., Thurston, M., Allende, S., Moodie, C., Dixon, M. L., Heimberg, R. G., & Gross, J. J. (2021). Evaluation of cognitive behavioral therapy vs mindfulness meditation in brain changes during reappraisal and acceptance among patients with social anxiety disorder. JAMA Psychiatry, 95817, 1–9. https://doi.org/10.1001/jamapsychiatry.2021.1862
Grabenhorst, F., & Schultz, W. (2021). Functions of primate amygdala neurons in economic decisions and social decision simulation. Behavioural Brain Research, 409, 113318. https://doi.org/10.1016/J.BBR.2021.113318
Gross, J. J. (2015). Emotion regulation: Current status and future prospects. Psychological Inquiry, 26(1), 1–26. https://doi.org/10.1080/1047840X.2014.940781
Gross, J. J., & Barrett, L. F. (2011). Emotion generation and emotion regulation: One or two depends on your point of view. Emotion Review, 3(1), 8–16. https://doi.org/10.1177/1754073910380974
Haxby, J. V., Gobbini, M. I., Furey, M. L., Ishai, A., Schouten, J. L., & Pietrini, P. (2001). Distributed and overlapping representations of faces and objects in ventral temporal cortex. Science, 293(5539), 2425–2430. https://doi.org/10.1126/science.1063736
Janak, P. H., & Tye, K. M. (2015). From circuits to behaviour in the amygdala. Nature, 517(7534), 284–292.
Knight, R. T., Richard Staines, W., Swick, D., & Chao, L. L. (1999). Prefrontal cortex regulates inhibition and excitation in distributed neural networks. Acta Psychologica, 101(2), 159–178. https://doi.org/10.1016/S0001-6918(99)00004-9
Kober, H., Barrett, L. F., Joseph, J., Bliss-Moreau, E., Lindquist, K., & Wager, T. D. (2008). Functional grouping and cortical-subcortical interactions in emotion: A meta-analysis of neuroimaging studies. NeuroImage, 42(2), 998–1031. https://doi.org/10.1016/j.neuroimage.2008.03.059
Kohn, N., Eickhoff, S. B., Scheller, M., Laird, A. R., Fox, P. T., & Habel, U. (2014). Neural network of cognitive emotion regulation—An ALE meta-analysis and MACM analysis. NeuroImage, 87, 345–355. https://doi.org/10.1016/j.neuroimage.2013.11.001
Kragel, P. A., Koban, L., Barrett, L. F., & Wager, T. D. (2018). Representation, pattern information, and brain signatures: From neurons to neuroimaging. Neuron, 99(2), 257–273. https://doi.org/10.1016/j.neuron.2018.06.009
LeDoux, J. (2012). Rethinking the emotional brain. Neuron, 73(4), 653–676.
Ledoux, J. E., & Brown, R. (2017). A higher-order theory of emotional consciousness. Proceedings of the National Academy of Sciences of the United States of America, 114(10), E2016–E2025. https://doi.org/10.1073/PNAS.1619316114/SUPPL_FILE/PNAS.1619316114.SAPP.PDF
Lindquist, K. A., Wager, T. D., Kober, H., Bliss-Moreau, E., & Barrett, L. F. (2012). The brain basis of emotion: A meta-analytic review. Behavioral and Brain Sciences, 35(3), 121–143. https://doi.org/10.1017/S0140525X11000446
Lindquist, K. A., & Barrett, L. F. (2012). A functional architecture of the human brain: Emerging insights from the science of emotion. Trends in Cognitive Sciences, 16(11). https://doi.org/10.1016/j.tics.2012.09.005
Lissek, S., Bradford, D. E., Alvarez, R. P., Burton, P., Espensen-Sturges, T., Reynolds, R. C., & Grillon, C. (2014). Neural substrates of classically conditioned fear-generalization in humans: A parametric fMRI study. Social Cognitive and Affective Neuroscience, 9(8), 1134–1142. https://doi.org/10.1093/SCAN/NST096
McRae, K., Hughes, B., Chopra, S., Gabrieli, J. D. E., Gross, J. J., & Ochsner, K. N. (2010). The neural bases of distraction and reappraisal. Journal of Cognitive Neuroscience, 22(2), 248–262. https://doi.org/10.1162/JOCN.2009.21243
McRae, K., Gross, J. J., Weber, J., Robertson, E. R., Sokol-Hessner, P., Ray, R. D., Gabrieli, J. D. E., & Ochsner, K. N. (2012a). The development of emotion regulation: An fMRI study of cognitive reappraisal in children, adolescents and young adults. Social Cognitive and Affective Neuroscience, 7(1), 11–22. https://doi.org/10.1093/scan/nsr093
McRae, K., Misra, S., Prasad, A. K., Pereira, S. C., & Gross, J. J. (2012b). Bottom-up and top-down emotion generation: Implications for emotion regulation. Social Cognitive and Affective Neuroscience, 7(3), 253–262. https://doi.org/10.1093/SCAN/NSQ103
Menon, V., & Uddin, L. Q. (2010). Saliency, switching, attention and control: A network model of insula function. Brain Structure & Function, 214(5–6), 655–667.
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24(1), 167–202. https://doi.org/10.1146/annurev.neuro.24.1.167
Morawetz, C., Bode, S., Baudewig, J., Jacobs, A. M., & Heekeren, H. R. (2016). Neural representation of emotion regulation goals. Human Brain Mapping, 37(2), 600–620. https://doi.org/10.1002/hbm.23053
Morawetz, C., Bode, S., Derntl, B., & Heekeren, H. R. (2017). The effect of strategies, goals and stimulus material on the neural mechanisms of emotion regulation: A meta-analysis of fMRI studies. Neuroscience and Biobehavioral Reviews, 72, 111–128. https://doi.org/10.1016/j.neubiorev.2016.11.014
Mur, M., Bandettini, P. A., & Kriegeskorte, N. (2009). Revealing representational content with pattern-information fMRI—an introductory guide. Social Cognitive and Affective Neuroscience, 4(1), 101–109. https://doi.org/10.1093/SCAN/NSN044
Norman, K. A., Polyn, S. M., Detre, G. J., & Haxby, J. V. (2006). Beyond mind-reading: Multi-voxel pattern analysis of fMRI data. Trends in Cognitive Sciences, 10(9), 424–430. https://doi.org/10.1016/J.TICS.2006.07.005
Ochsner, K. N., Silvers, J. A., & Buhle, J. T. (2012). Functional imaging studies of emotion regulation: A synthetic review and evolving model of the cognitive control of emotion. Annals of the new York Academy of Sciences, 1251(1), E1–E24.
Ochsner, K. N., & Gross, J. J. (2005). The cognitive control of emotion. Trends in Cognitive Sciences, 9(5), 242–249. https://doi.org/10.1016/J.TICS.2005.03.010
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. E. (2002). Rethinking feelings: An fMRI study of the cognitive regulation of emotion. Journal of Cognitive Neuroscience, 14(8), 1215–1229. https://doi.org/10.1162/089892902760807212
Ochsner, K. N., Ray, R. D., Cooper, J. C., Robertson, E. R., Chopra, S., Gabrieli, J. D. E., & Gross, J. J. (2004). For better or for worse: Neural systems supporting the cognitive down- and up-regulation of negative emotion. NeuroImage, 23(2), 483–499. https://doi.org/10.1016/j.neuroimage.2004.06.030
Ochsner, K. N., Ray, R. R., Hughes, B., Mcrae, K., Cooper, J. C., Weber, J., Gabrieli, J. D. E., & Gross, J. J. (2009). Bottom-up and top-down processes in emotion generation: Common and distinct neural mechanisms. Psychological Science, 20(11), 1322–1331. https://doi.org/10.1111/j.1467-9280.2009.02459.x
Olofsson, J. K., Nordin, S., Sequeira, H., & Polich, J. (2008). Affective picture processing: An integrative review of ERP findings. Biological Psychology, 77(3), 247–265.
Paton, J. J., Belova, M. A., Morrison, S. E., & Salzman, C. D. (2006). The primate amygdala represents the positive and negative value of visual stimuli during learning. Nature, 439(7078), 865–870.
Pessoa, L. (2010). Emotion and cognition and the amygdala: From “what is it?” to “what’s to be done?” Neuropsychologia, 48(12), 3416–3429. https://doi.org/10.1016/J.NEUROPSYCHOLOGIA.2010.06.038
Phillips, M. L., Drevets, W. C., Rauch, S. L., & Lane, R. (2003). Neurobiology of emotion perception I: The neural basis of normal emotion perception. Biological Psychiatry, 54(5), 504–514. https://doi.org/10.1016/S0006-3223(03)00168-9
Poldrack, R. A. (2006). Can cognitive processes be inferred from neuroimaging data? Trends in Cognitive Sciences, 10(2), 59–63. https://doi.org/10.1016/J.TICS.2005.12.004
Poldrack, R. A. (2011). Inferring mental states from neuroimaging data: From reverse inference to large-scale decoding. Neuron, 72(5), 692–697. https://doi.org/10.1016/J.NEURON.2011.11.001
Quirk, G. J., Garcia, R., & González-Lima, F. (2006). Prefrontal mechanisms in extinction of conditioned fear. Biological Psychiatry, 60(4), 337–343. https://doi.org/10.1016/J.BIOPSYCH.2006.03.010
Schmitz, T. W., & Johnson, S. C. (2007). Relevance to self: A brief review and framework of neural systems underlying appraisal. Neuroscience & Biobehavioral Reviews, 31(4), 585–596. https://doi.org/10.1016/J.NEUBIOREV.2006.12.003
Shabel, S. J., & Janak, P. H. (2009). Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal. Proceedings of the National Academy of Sciences, 106(35), 15031–15036.
Thiruchselvam, R., Blechert, J., Sheppes, G., Rydstrom, A., & Gross, J. J. (2011). The temporal dynamics of emotion regulation: An EEG study of distraction and reappraisal. Biological Psychology, 87(1), 84–92. https://doi.org/10.1016/j.biopsycho.2011.02.009
Urry, H. L., Van Reekum, C. M., Johnstone, T., Kalin, N. H., Thurow, M. E., Schaefer, H. S., Jackson, C. A., Frye, C. J., Greischar, L. L., Alexander, A. L., & Davidson, R. J. (2006). Amygdala and ventromedial prefrontal cortex are inversely coupled during regulation of negative affect and predict the diurnal pattern of cortisol secretion among older adults. Journal of Neuroscience, 26(16), 4415–4425. https://doi.org/10.1523/JNEUROSCI.3215-05.2006
Urry, H. L., Van Reekum, C. M., Johnstone, T., & Davidson, R. J. (2009). Individual differences in some (but not all) medial prefrontal regions reflect cognitive demand while regulating unpleasant emotion. NeuroImage, 47, 852–863. https://doi.org/10.1016/j.neuroimage.2009.05.069
van Reekum, C. M., Johnstone, T., Urry, H. L., Thurow, M. E., Schaefer, H. S., Alexander, A. L., & Davidson, R. J. (2007). Gaze fixations predict brain activation during the voluntary regulation of picture-induced negative affect. NeuroImage, 36(3), 1041–1055. https://doi.org/10.1016/J.NEUROIMAGE.2007.03.052
Vigneau, M., Beaucousin, V., Hervé, P. Y., Duffau, H., Crivello, F., Houdé, O., Mazoyer, B., & Tzourio-Mazoyer, N. (2006). Meta-analyzing left hemisphere language areas: Phonology, semantics, and sentence processing. NeuroImage, 30(4), 1414–1432. https://doi.org/10.1016/J.NEUROIMAGE.2005.11.002
Wager, T. D., Davidson, M. L., Hughes, B. L., Lindquist, M. A., & Ochsner, K. N. (2008). Prefrontal-subcortical pathways mediating successful emotion regulation. Neuron, 59(6), 1037–1050. https://doi.org/10.1016/j.neuron.2008.09.006
Wager, T. D., & Barrett, L. F. (2017). From affect to control: Functional specialization of the insula in motivation and regulation. bioRxiv, 102368. https://doi.org/10.1101/102368
Wager, T. D., & Smith, E. E. (2003). Neuroimaging studies of working memory. Cognitive, Affective, & Behavioral Neuroscience, 3, 255–274.
Westlin, C., Theriault, J. E., Katsumi, Y., Nieto-Castanon, A., Kucyi, A., Ruf, S. F., Brown, S. M., Pavel, M., Erdogmus, D., Brooks, D. H., Quigley, K. S., Whitfield-Gabrieli, S., & Barrett, L. F. (2023). Improving the study of brain-behavior relationships by revisiting basic assumptions. Trends in Cognitive Sciences, 27(3), 246–257. https://doi.org/10.1016/j.tics.2022.12.015
Zhang, J., Lau, E. Y. Y., & Hsiao, J. H. (2019). Using emotion regulation strategies after sleep deprivation: ERP and behavioral findings. Cognitive, Affective, & Behavioral Neuroscience, 19(2), 283–295. https://doi.org/10.3758/s13415-018-00667-y
Zhang, J.-X., Kurian, A. W., Jo, B., Nouriani, B., Neri, E., Gross, J. J., & Spiegel, D. (2023). Emotion regulation and choice of bilateral mastectomy for the treatment of unilateral breast cancer. Cancer Medicine, 12(11), 12837–12846. https://doi.org/10.1002/cam4.5963
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Funding for this research was provided by National Institute of Health (NIH) grants CA197282 and MH092416.
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JXZ, MLD, and JJG conceptualized the research. JXZ analyzed and visualized the data. JXZ wrote the original draft. All authors provided critical revisions.
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Zhang, JX., Dixon, M.L., Goldin, P.R. et al. The Neural Separability of Emotion Reactivity and Regulation. Affec Sci 4, 617–629 (2023). https://doi.org/10.1007/s42761-023-00227-9
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DOI: https://doi.org/10.1007/s42761-023-00227-9