Trait self-compassion enhances activation in the medial prefrontal cortex during fear extinction: an fNIRS study

• Tingyuan Chen ^[1] ; Ying Mei ^[1] ; Siyuan Zhou ^[1] ; Haoran Dou ^[1] ; Yi Lei ^[1]
  1. [1] Sichuan Normal University

     Sichuan Normal University

     China

     
• Localización: International journal of clinical and health psychology, ISSN 1697-2600, Vol. 24, Nº. 4, 2024, págs. 131-140
• Idioma: inglés
• DOI: 10.1016/j.ijchp.2024.100516
• Enlaces
  • Texto completo
• Resumen

  • Fear acquisition and fear extinction are the most widely used experimental models to study anxiety related disorders, with the medial prefrontal cortex (mPFC) playing an important role in this process. Previous research suggests that trait self-compassion is associated with lower anxiety, but the neural mechanisms underlying this relationship remain unclear. Women generally exhibit lower self-compassion than men, making them more vulnerable to fear and anxiety. In this study, female participants were divided into two groups - high and low trait self-compassion, based on their scores on the Self-Compassion Scale-Short Form (SCS-SF). Both groups completed fear acquisition and fear extinction tasks, during which conditioned responses (CRs) were measured using self-reported unconditioned stimulus (US) expectancy ratings, skin conductance response (SCR), and functional near-infrared spectroscopy (fNIRS). The results showed that in the fear acquisition phase, all participants successfully acquired fear, showing greater responses to threat stimuli than safety stimuli. However, participants with high trait self-compassion exhibited lower SCR than those with low trait self-compassion. In the fear extinction phase, compared to individuals with low trait self-compassion, individuals with high trait self-compassion exhibited more effective fear extinction learning, characterized by lower US expectancy ratings, lower SCR, and higher mPFC activation. Moreover, trait self-compassion was significantly correlated with the behavioral extinction ability and the mPFC activation during the late phase of fear extinction, and behavioral extinction ability was significantly correlated with mPFC activation. The findings of this study suggest individuals with high trait self-compassion have better physiological flexibility during fear acquisition and fear extinction, and may through enhancing mPFC activation to facilitate fear extinction. The results provide new insights into the pathological mechanisms of anxiety.

• Referencias bibliográficas
  • Abend, R., Gold, A. L., Britton, J. C., Michalska, K. J., Shechner, T., Sachs, J. F., et al. (2020). Anticipatory threat responding: Associations...
  • Abend, R., Sar-El, R., Gonen, T., Jalon, I., Vaisvaser, S., Bar-Haim, Y., et al. (2019). Modulating emotional experience using electrical...
  • Alexandra Kredlow, M., Pineles, S. L., Inslicht, S. S., Marin, M.-F., Milad, M. R., Otto, M. W., et al. (2017). Assessment of skin conductance...
  • Allen, A. B., & Leary, M. R. (2010). Self-Compassion, stress, and coping. Social and Personality Psychology Compass, 4(2), 107–118. https://doi.org/10.1111/j.1751-9004.2009.00246.x
  • Balada, F., Aluja, A., García, O., Aymamí, N., & García, L. F. (2024). Gender Differences in Prefrontal Cortex Response to Negative Emotional...
  • Barrett, J., & Armony, J. (2009). Influence of trait anxiety on brain activity during the acquisition and extinction of aversive conditioning....
  • Beckers, T., Hermans, D., Lange, I., Luyten, L., Scheveneels, S., & Vervliet, B. (2023). Understanding clinical fear and anxiety through...
  • Measures, S. for P. R. A. H. C. on E., Boucsein, W., Fowles, D. C., Grimnes, S., Ben- Shakhar, G., Roth, W. T., Dawson, M. E., et al. (2012)....
  • Bradley, M. M., & Lang, P. J. (1999). International affective digitized sounds (IADS): Stimuli, instruction manual and affective ratings...
  • Breines, J. G., & Chen, S. (2012). Self-compassion increases self-improvement motivation. Personality and Social Psychology Bulletin,...
  • Breines, J. G., McInnis, C. M., Kuras, Y. I., Thoma, M. V., Gianferante, D., Hanlin, L., et al. (2015). Self-compassionate young adults show...
  • Constantinou, E., Purves, K. L., McGregor, T., Lester, K. J., Barry, T. J., Treanor, M., et al. (2021). Measuring fear: Association among...
  • Creaser, J. L., Storr, J., & Karl, A. (2022). Brain Responses to a Self-Compassion Induction in Trauma Survivors With and Without Post-traumatic...
  • Dibbets, P., van den Broek, A., & Evers, E. A. (2015). Fear conditioning and extinction in anxiety-and depression-prone persons. Memory...
  • Dos Santos, F. R. M., Bazan, P. R., Balardin, J. B., De Aratanha, M. A., Rodrigues, M., Lacerda, S., et al. (2022). Changes in Prefrontal...
  • Dou, H., Lei, Y., Cheng, X., Wang, J., & Leppa¨nen, P. H. (2020). Social exclusion influences conditioned fear acquisition and generalization:...
  • Eichholz, A., Schwartz, C., Meule, A., Heese, J., Neumüller, J., & Voderholzer, U. (2020). Self-compassion and emotion regulation difficulties...
  • Etkin, A., Egner, T., & Kalisch, R. (2011). Emotional processing in anterior cingulate and medial prefrontal cortex. Trends in Cognitiveences,...
  • Fullana Rivas, M.A., Harrison, B. J., Soriano Mas, C., Vervliet, B., Cardoner, N., A`vila- Parcet, A., et al. (2016). Neural signatures...
  • Gervain, J., Mehler, J., Werker, J. F., Nelson, C. A., Csibra, G., Lloyd-Fox, S., et al. (2011). Near-infrared spectroscopy: A report from...
  • Giustino, T. F., & Maren, S. (2015). The role of the medial prefrontal cortex in the conditioning and extinction of fear. Frontiers in...
  • Gong, H., Jia, H., Guo, T., & Zou, L. (2014). The revision of self-compassion scale and its reliability and validity in adolescents. Psychological...
  • Greco, J. A., & Liberzon, I. (2016). Neuroimaging of fear-associated learning. Neuropsychopharmacology : official publication of the American...
  • Guan, F., Liu, G., Pedersen, W. S., Chen, O., Zhao, S., Sui, J., et al. (2021). Neurostructural correlates of dispositional self-compassion....
  • Guhn, A., Dresler, T., Hahn, T., Mühlberger, A., Stro¨hle, A., Deckert, J., et al. (2012). Medial prefrontal cortex activity during the extinction...
  • Herry, C., Ferraguti, F., Singewald, N., Letzkus, J. J., Ehrlich, I., & Lüthi, A. (2010). Neuronal circuits of fear extinction. European...
  • Hornstein, E. A., Fanselow, M. S., & Eisenberger, N. I. (2016). A safe haven: Investigating social-support figures as prepared safety...
  • Jafari, E., Alizadehgoradel, J., Koluri, F. P., Nikoozadehkordmirza, E., Refahi, M., Taherifard, M., et al. (2021). Intensified electrical...
  • Jasper, H. (1958). The 10-20 electrode system of the International Federation. Electroencephalogr Clin Neuropysiol, 10, 370–375.
  • Kenwood, M. M., Kalin, N. H., & Barbas, H. (2022). The prefrontal cortex, pathological anxiety, and anxiety disorders. Neuropsychopharmacology...
  • Kirschner, H., Kuyken, W., & Karl, A. (2022). A biobehavioural approach to understand how mindfulness-based cognitive therapy reduces...
  • Kirschner, H., Kuyken, W., Wright, K., Roberts, H., Brejcha, C., & Karl, A. (2019). Soothing your heart and feeling connected: A new experimental...
  • Klein, Z., Berger, S., Vervliet, B., & Shechner, T. (2021). Fear learning, avoidance, and generalization are more context-dependent for...
  • Kruse, O., Tapia Leon, I., Stark, R., & Klucken, T. (2017). Neural correlates of appetitive extinction in humans. Social Cognitive and...
  • Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., et al. (2000). Automated Talairach atlas labels...
  • Laurent, V., & Westbrook, R. F. (2009). Inactivation of the infralimbic but not the prelimbic cortex impairs consolidation and retrieval...
  • Leary, M. R., Tate, E. B., Adams, C. E., Batts Allen, A., & Hancock, J. (2007). Self- compassion and reactions to unpleasant self-relevant...
  • Lei, Z., Bi, R., Mo, L., Yu, W., & Zhang, D. (2021). The brain mechanism of explicit and implicit processing of affective prosodies: An...
  • Lipp, O. V. (2006). Human Fear Learning: Contemporary Procedures and Measurement. In M. G. Craske, D. Hermans, & D. Vansteenwegen (Eds.),...
  • Luo, X., Qiao, L., & Che, X. (2018). Self-compassion modulates heart rate variability and negative affect to experimentally induced stress....
  • Lutz, J., Berry, M. P., Napadow, V., Germer, C., Pollak, S., Gardiner, P., et al. (2020). Neural activations during self-related processing...
  • MacBeth, A., & Gumley, A. (2012). Exploring compassion: A meta-analysis of the association between self-compassion and psychopathology....
  • Maier, S., Szalkowski, A., Kamphausen, S., Perlov, E., Feige, B., Blechert, J., et al. (2012). Clarifying the role of the rostral dmPFC/dACC...
  • Malik, S., & Perveen, A. (2023). Mindfulness and anxiety among university students: Moderating role of cognitive emotion regulation. Current...
  • McNally, R. J. (2007). Mechanisms of exposure therapy: How neuroscience can improve psychological treatments for anxiety disorders. Clinical...
  • Mcrae, K., Ochsner, K. N., Mauss, I. B., Gabrieli, J. J. D., & Gross, J. J. (2008). Gender Differences in Emotion Regulation: An fMRI...
  • Mei, Y., Liu, J., Liu, H., Fu, Y., Luo, X., & Lei, Y. (2023). Self-compassion writing facilitates fear extinction. Acta Psychologica Sinica,...
  • Michalska, K. J., Machlin, L., Moroney, E., Lowet, D. S., Hettema, J. M., Roberson- Nay, R., et al. (2017). Anxiety symptoms and children’s...
  • Milad, M. R., Goldstein, J. M., Orr, S. P., Wedig, M. M., Klibanski, A., Pitman, R. K., et al. (2006). Fear conditioning and extinction: Influence...
  • Milad, M. R., Wright, C. I., Orr, S. P., Pitman, R. K., Quirk, G. J., & Rauch, S. L. (2007). Recall of fear extinction in humans activates...
  • Molavi, B., & Dumont, G. A. (2012). Wavelet-based motion artifact removal for functional near-infrared spectroscopy. Physiological Measurement,...
  • Muris, P., & Petrocchi, N. (2017). Protection or vulnerability? A meta-analysis of the relations between the positive and negative components...
  • Neff, K. D. (2003a). Self-compassion: An alternative conceptualization of a healthy attitude toward oneself. Self and Identity, 2(2), 85–101....
  • Neff, K. D. (2003b). The development and validation of a scale to measure self- compassion. Self and Identity, 2(3), 223–250. https://doi.org/10.1080/...
  • Neff, K. D., & Dahm, K. A. (2015). Self-Compassion: What It Is, What It Does, and How It Relates to MindfulnessB. D. Ostafin, M. D. Robinson,...
  • Neff, K. D., & Germer, C. K. (2012). A pilot study and randomized controlled trial of the mindful self-compassion program. Journal of...
  • Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. (2002). Rethinking feelings: An FMRI study of the cognitive regulation of...
  • Parrish, M. H., Inagaki, T. K., Muscatell, K. A., Haltom, K. E., Leary, M. R., & Eisenberger, N. I. (2018). Self-compassion and responses...
  • Pinti, P., Tachtsidis, I., Hamilton, A., Hirsch, J., Aichelburg, C., Gilbert, S., et al. (2020). The present and future use of functional...
  • Piper, S. K., Krueger, A., Koch, S. P., Mehnert, J., Habermehl, C., Steinbrink, J., et al. (2014). A wearable multi-channel fNIRS system for...
  • Saviola, F., Pappaianni, E., Monti, A., Grecucci, A., Jovicich, J., & De Pisapia, N. (2020). Trait and state anxiety are mapped differently...
  • Singh, S., & Topolnik, L. (2023). Inhibitory circuits in fear memory and fear-related disorders. Frontiers in Neural Circuits, 17, Article...
  • Spielberger, C. D. (1970). Manual for the State-Trait Anxiety Inventory. Self Evaluation Questionnaire.
  • Suzuki, Y., & Tanaka, S. C. (2021). Functions of the ventromedial prefrontal cortex in emotion regulation under stress. Scientific Reports,...
  • Svendsen, J. L., Osnes, B., Binder, P.-E., Dundas, I., Visted, E., Nordby, H., et al. (2016). Trait self-compassion reflects emotional flexibility...
  • Svendsen, J. L., Schanche, E., Osnes, B., Vøllestad, J., Visted, E., Dundas, I., et al. (2020). Is dispositional self-compassion associated...
  • Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective...
  • Tong, Y., Hocke, L. M., & Frederick, B.deB. (2011). Isolating the sources of widespread physiological fluctuations in functional near-infrared...
  • Tovote, P., Fadok, J. P., & Lüthi, A. (2015). Neuronal circuits for fear and anxiety. Nature Reviews Neuroscience, 16(6), 317–331. https://doi.org/10.1038/nrn3945
  • Treanor, M., Rosenberg, B. M., & Craske, M. G. (2021). Pavlovian learning processes in pediatric anxiety disorders: A critical review....
  • Van der Horn, H. J., Liemburg, E. J., Aleman, A., Spikman, J. M., & van der Naalt, J. (2016). Brain networks subserving emotion regulation...
  • Vervliet, B., Lange, I., & Milad, M. R. (2017). Temporal dynamics of relief in avoidance conditioning and fear extinction: Experimental...
  • Vicario, C. M., Nitsche, M. A., Hoysted, I., Yavari, F., Avenanti, A., Salehinejad, M. A., et al. (2020). Anodal transcranial direct current...
  • Vriends, N., Michael, T., Blechert, J., Meyer, A. H., Margraf, J., & Wilhelm, F. H. (2011). The influence of state anxiety on the acquisition...
  • Wang, H., Zhang, X., Si, C., Xu, Y., Liu, Q., Bian, H.-T., et al. (2018). Prefrontoparietal dysfunction during emotion regulation in anxiety...
  • Yarnell, L. M., Stafford, R. E., Neff, K. D., Reilly, E. D., Knox, M. C., & Mullarkey, M. (2015). Meta-analysis of gender differences...
  • Zhang, J., Wu, Y., Chen, X., & Liu, D. (2014). Probabilistic implicit sequence learning differences between individuals with high vs....