Abstract
Objectives
The aim of this study was to investigate the effects of self-compassionate thinking (SCT) related to stressful autobiographical memories (SAM) on the prefrontal cortex (PFC) activity and heart rate variability (HRV) parameters in healthy subjects.
Methods
A naturalistic paradigm was built with two conditions, SAM followed by SCT. We used functional near-infrared spectroscopy (fNIRS) to measure oxy and deoxyhemoglobin concentration changes in 33 healthy adults (men = 10) with a mean age of 33.24 years (SD = 6.85). Two HRV parameters were also measured during both conditions: the standard deviations of the normal-to-normal (SDNN-HRV) and the high-frequency component of heart rate variability (HF-HRV).
Results
During the SAM condition, the left dorsolateral PFC (DLPFC) and the frontopolar area showed a significantly increased oxyhemoglobin concentration compared with the control condition (corrected-p < 0.01). During the SCT condition, the frontopolar area showed a significantly increased oxyhemoglobin compared with the control condition (corrected-p < 0.001). A significant increase in time-domain SDNN-HRV (p = 0.002) during SCT compared with the SAM condition was also observed. An association between the frontopolar area fNIRS signal and the HF-HRV during SAM condition was found (corrected-p < 0.05).
Conclusions
Our findings suggested that the SAM condition is associated with activity in the left DLPFC and in the frontopolar area, while the SCF is associated with activity in the frontopolar area. The SCT was related to an increase in SDNN-HRV when compared with the SAM condition, and an association between HF-HRV and PFC activity was seen. Our results also suggested that self-compassionate thinking can be an effective emotional regulation strategy.
Trial Registration
Clinical Trials NCT03737084.
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Data Availability
The authors will share data from the study upon reasonable request to the corresponding author.
Change history
28 March 2022
A Correction to this paper has been published: https://doi.org/10.1007/s12671-022-01871-1
References
Allen, B., Jennings, J. R., Gianaros, P. J., Thayer, J. F., & Manuck, S. B. (2015). Resting high-frequency heart rate variability is related to resting brain perfusion. Psychophysiology, 52(2), 277–287. https://doi.org/10.1111/psyp.12321.
Balardin, J. B., Zimeo Morais, G. A., Furucho, R. A., Trambaiolli, L., Vanzella, P., Biazoli, C., Jr., & Sato, J. R. (2017). Imaging brain function with functional near-infrared spectroscopy in unconstrained environments. Frontiers in Human Neuroscience, 11, 258. https://doi.org/10.3389/fnhum.2017.00258.
Barker, J. W., Aarabi, A., & Huppert, T. J. (2013). Autoregressive model based algorithm for correcting motion and serially correlated errors in fNIRS. Biomedical Optics Express, 4(8), 1366–1379. https://doi.org/10.1364/BOE.4.001366.
Chand, T., Li, M., Jamalabadi, H., Wagner, G., Lord, A., Alizadeh, S., … Sen, Z. D. (2020). Heart rate variability as an index of differential brain dynamics at rest and after acute stress induction. Frontiers in Neuroscience, 14, 645. https://doi.org/10.3389/fnins.2020.00645.
Compare, A., Brugnera, A., Adorni, R., & Sakatani, K. (2016). Effects of positive and negative mood induction on the prefrontal cortex activity measured by near infrared spectroscopy. Advances in Experimental Medicine and Biology, 923, 151–157. https://doi.org/10.1007/978-3-319-38810-6_20.
Conway, M. A., Pleydell-Pearce, C. W., & Whitecross, S. E. (2001). The neuroanatomy of autobiographical memory: A slow cortical potential study of autobiographical memory retrieval. Journal of Memory and Language, 45(3), 493–524. https://doi.org/10.1006/jmla.2001.2781.
Davidson, R. J. (2004). What does the prefrontal cortex “do” in affect: Perspectives on frontal EEG asymmetry research. Biological Psychology, 67(1–2), 219–234. https://doi.org/10.1016/j.biopsycho.2004.03.008.
Davidson, R. J., & Fox, N. A. (1982). Asymmetrical brain activity discriminates between positive and negative affective stimuli in human infants. Science, 218(4578), 1235–1237. https://doi.org/10.1126/science.7146906.
Elias, M. F., & Torres, R. V. (2017). The renaissance of heart rate variability as a predictor of cognitive functioning. American Journal of Hypertension, 31(1), 21–23. https://doi.org/10.1093/ajh/hpx150.
Gilbert, P. (2010). Compassion focused therapy: Distinctive features. Routledge/Taylor & Francis Group.
Grossman, P., & Taylor, E. W. (2007). Toward understanding respiratory sinus arrhythmia: Relations to cardiac vagal tone, evolution and biobehavioral functions. Biological Psychology, 74(2), 263–285. https://doi.org/10.1016/j.biopsycho.2005.11.014.
Holzman, J. B., & Bridgett, D. J. (2017). Heart rate variability indices as bio-markers of top-down self-regulatory mechanisms: A meta-analytic review. Neuroscience & Biobehavioral Reviews, 74, 233–255. https://doi.org/10.1016/j.neubiorev.2016.12.032.
Huppert, T. J. (2016). Commentary on the statistical properties of noise and its implication on general linear models in functional near-infrared spectroscopy. Neurophotonics, 3(1), 010401. https://doi.org/10.1117/1.NPh.3.1.010401.
Hutcherson, C. A., Plassmann, H., Gross, J. J., & Rangel, A. (2012). Cognitive regulation during decision making shifts behavioral control between ventromedial and dorsolateral prefrontal value systems. Journal of Neuroscience, 32(39), 13543–13554. https://doi.org/10.1523/JNEUROSCI.6387-11.2012.
Johnson, S. C., Baxter, L. C., Wilder, L. S., Pipe, J. G., Heiserman, J. E., & Prigatano, G. P. (2002). Neural correlates of self-reflection. Brain, 125(8), 1808–1814. https://doi.org/10.1093/brain/awf181.
Kim, J. J., Parker, S. L., Doty, J. R., Cunnington, R., Gilbert, P., & Kirby, J. N. (2020). Neurophysiological and behavioural markers of compassion. Scientific Reports, 10(1), 1–9. https://doi.org/10.1038/s41598-020-63846-3.
Lane, R. D., McRae, K., Reiman, E. M., Chen, K., Ahern, G. L., & Thayer, J. F. (2009). Neural correlates of heart rate variability during emotion. Neuroimage, 44(1), 213–222. https://doi.org/10.1016/j.neuroimage.2008.07.056.
Li, Y., Grabell, A. S., Wakschlag, L. S., Huppert, T. J., & Perlman, S. B. (2017). The neural substrates of cognitive flexibility are related to individual differences in preschool irritability: A fNIRS investigation. Developmental Cognitive Neuroscience, 25, 138–144. https://doi.org/10.1016/j.dcn.2016.07.002.
Luo, X., Qiao, L., & Che, X. (2018). Self-compassion modulates heart rate variability and negative affect to experimentally induced stress. Mindfulness, 9(5), 1522–1528. https://doi.org/10.1007/s12671-018-0900-9.
Luo, X., Liu, J., & Che, X. (2020). Investigating the influence and a potential mechanism of self-compassion on experimental pain: evidence from a compassionate self-talk protocol and heart rate variability. The Journal of Pain, 21(7-8), 790–797. https://doi.org/10.1016/j.jpain.2019.11.006.
Maguire, E. A. (2001). Neuroimaging studies of autobiographical event memory. The Royal Society: Philosophical Transactions: Biological Sciences, 1413, 1441–1451. https://doi.org/10.1098/rstb.2001.0944.
Maier, S. U., & Hare, T. A. (2017). Higher heart-rate variability is associated with ventromedial prefrontal cortex activity and increased resistance to temptation in dietary self-control challenges. Journal of Neuroscience, 37(2), 446–455. https://doi.org/10.1523/JNEUROSCI.2815-16.2016.
McCraty, R., & Shaffer, F. (2015). Heart rate variability: New perspectives on physiological mechanisms, assessment of self-regulatory capacity, and health risk. Global Advances in Health and Medicine, 4, 46–61. https://doi.org/10.7453/gahmj.2014.073.
Miller, E. K., & Cohen, J. D. (2001). An integrative theory of prefrontal cortex function. Annual Review of Neuroscience, 24, 67–202. https://doi.org/10.1146/annurev.neuro.24.1.167.
Morais, G. A. Z., Balardin, J. B., & Sato, J. R. (2018). fNIRS optodes’ location decider (fOLD): A toolbox for probe arrangement guided by brain regions-of-interest. Scientific Reports, 8(1), 1–11. https://doi.org/10.1038/s41598-018-21716-z.
Motzkin, J. C., Philippi, C. L., Wolf, R. C., Baskaya, M. K., & Koenigs, M. (2015). Ventromedial prefrontal cortex is critical for the regulation of amygdala activity in humans. Biological Psychiatry, 77(3), 276–284. https://doi.org/10.1016/j.biopsych.2014.02.014.
Neff, K. D. (2003). Self-compassion: An alternative conceptualization of a healthy attitude toward oneself. Self and Identity, 2(2), 85–101. https://doi.org/10.1080/15298860309032.
Nikolin, S., Boonstra, T. W., Loo, C. K., & Martin, D. (2017). Combined effect of prefrontal transcranial direct current stimulation and a working memory task on heart rate variability. PLoS ONE, 12, e0181833. https://doi.org/10.1371/journal.pone.0181833.
Ochsner, K. N., Bunge, S. A., Gross, J. J., & Gabrieli, J. D. (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.
Park, G., Vasey, M. W., Van Bavel, J. J., & Thayer, J. F. (2013). Cardiac vagal tone is correlated with selective attention to neutral distractors under load. Psychophysiology, 50(4), 398–406. https://doi.org/10.1111/psyp.12029.
Petrocchi, N., Ottaviani, C., & Couyoumdjian, A. (2017). Compassion at the mirror: Exposure to a mirror increases the efficacy of a self-compassion manipulation in enhancing soothing positive affect and heart rate variability. The Journal of Positive Psychology, 12(6), 525–536. https://doi.org/10.1080/17439760.2016.1209544.
Riedel, P., Heil, M., Bender, S., Dippel, G., Korb, F. M., Smolka, M. N., & Marxen, M. (2019). Modulating functional connectivity between medial frontopolar cortex and amygdala by inhibitory and excitatory transcranial magnetic stimulation. Human Brain Mapping, 40(15), 4301–4315. https://doi.org/10.1002/hbm.24703.
Rorden, C., & Brett, M. (2000). Stereotaxic display of brain lesions. Behavioural Neurology, 12(4), 191–200. https://doi.org/10.1155/2000/421719.
Rosenbaum, D., Hilsendegen, P., Thomas, M., Haeussinger, F. B., Metzger, F. G., Nuerk, H. C., … Ehlis, A. C. (2018). Cortical hemodynamic changes during the trier social stress test: An fNIRS study. NeuroImage, 171, 107–115. https://doi.org/10.1016/j.neuroimage.2017.12.061.
Salo, M. A., Huikuri, H. V., & Seppanen, T. (2001). Ectopic beats in heart rate variability analysis: Effects of editing on time and frequency domain measures. Annals of Noninvasive Electrocardiology, 6(1), 5–17. https://doi.org/10.1111/j.1542-474X.2001.tb00080.x.
Santosa, H., Zhai, X., Fishburn, F., & Huppert, T. (2018). The NIRS Brain AnalyzIR Toolbox. Algorithms, 11(5), 73. https://doi.org/10.3390/a11050073.
Schaal, N. K., Hepp, P., Schweda, A., Wolf, O. T., & Krampe, C. (2019). A functional near-infrared spectroscopy study on the cortical haemodynamic responses during the Maastricht acute stress test. Scientific Reports, 9(1), 1–11. https://doi.org/10.1038/s41598-019-49826-2.
Shaffer, F., & Ginsberg, J. P. (2017). An overview of heart rate variability metrics and norms. Frontiers in Public Health, 5, 258. https://doi.org/10.3389/fpubh.2017.00258.
Scholkmann, F., & Wolf, M. (2013). General equation for the differential pathlength factor of the frontal human head depending on wavelength and age. Journal of Biomedical Optics, 18(10), 105004. https://doi.org/10.1117/1.JBO.18.10.105004.
Stellar, J. E., Cohen, A., Oveis, C., & Keltner, D. (2015). Affective and physiological responses to the suffering of others: Compassion and vagal activity. Journal of Personality and Social Psychology, 108(4), 572. https://doi.org/10.1037/pspi0000010.
Svendsen, J. L., Osnes, B., Binder, P. E., Dundas, I., Visted, E., Nordby, H., … Sørensen, L. (2016). Trait self-compassion reflects emotional flexibility through an association with high vagally mediated heart rate variability. Mindfulness, 7(5), 1103–1113. https://doi.org/10.1007/s12671-018-1007-z.
Svoboda, E., McKinnon, M. C., & Levine, B. (2006). The functional neuroanatomy of autobiographical memory: A meta-analysis. Neuropsychologia, 44(12), 2189–2208. https://doi.org/10.1016/j.neuropsychologia.2006.05.023.
Tarvainen, M. P., Niskanen, J. P., Lipponen, J. A., Ranta-Aho, P. O., & Karjalainen, P. A. (2014). Kubios HRV–heart rate variability analysis software. Computer Methods and Programs in Biomedicine, 113(1), 210–220. https://doi.org/10.1016/j.cmpb.2013.07.024.
Task force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. (1996). Heart rate variability: Standards of measurement, physiological interpretation and clinical use. Circulation, 93(5), 1043–1065. https://doi.org/10.1161/01.CIR.93.5.1043.
Thayer, J. F., & Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. Journal of Affective Disorders, 61(3), 201–216. https://doi.org/10.1016/S0165-0327(00)00338-4.
Thayer, J. F., Ahs, F., Fredrikson, M., Sollers, J. J., III., & Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: Implications for heart rate variability as a marker of stress and health. Neuroscience and Biobehavioral Reviews, 36, 747–756. https://doi.org/10.1016/j.neubiorev.2011.11.009.
Acknowledgements
We would like to thank Lama Rinchen Kyenrab for his contribution to the self-compassionate thinking narrative, and also thank Jose Belem de Oliveira Neto for the English review.
Funding
The project was supported by funding provided by Natura Cosméticos S.A. and Instituto Israelita de Ensino e Pesquisa Albert Einstein.
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FRMS: designed and executed the study, collected data, composed and edited the manuscript. PRB: analyzed the data and wrote part of the results and discussion. JBB: collaborated with the design of the study. MAA: collaborated with the design of the study. MR: collaborated with the design of the study. SL: collaborated with the design of the study and analyzed part of the data. GLTN: collaborated with the design of the study. EHK: provided supervision, collaborated with the design of the study and writing of the manuscript. All authors read and approved the final manuscript.
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This trial is registered at Clinical Trials: NCT03737084. It was approved by the Ethics Committee in Research of Hospital Israelita Albert Einstein, number: 79179417.4.0000.0071 and follow ethical standards of the Helsinki Declaration of 1964 and its later amendments.
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Informed consent was obtained from all participants who participated in the study.
Conflict of Interest
Maria Adelia de Aratanha is employed by NIRx Medizintechnik GmbH. Paulo Rodrigo Bazán provides scientific consulting to Brain Support Corporation, which is a distributor of NIRx Medizintechnik GmbH.
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dos Santos, F.R.M., Bazán, P.R., Balardin, J.B. et al. Changes in Prefrontal fNIRS Activation and Heart Rate Variability During Self-Compassionate Thinking Related to Stressful Memories. Mindfulness 13, 326–338 (2022). https://doi.org/10.1007/s12671-021-01789-0
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DOI: https://doi.org/10.1007/s12671-021-01789-0