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Coping with Emotions Past: The Neural Bases of Regulating Affect Associated with Negative Autobiographical Memories
Open accessAbstract
Background Although the ability to adaptively reflect on negative autobiographical experiences without ruminating is critical to mental health, to our knowledge no research has directly examined the neural systems underlying this process.Methods Sixteen participants were scanned using functional magnetic resonance imaging (fMRI) as they focused on negative autobiographical memories using cognitive strategies designed to facilitate (feel strategy) versus undermine (analyze and accept strategies) rumination.Results Two key findings were obtained. First, consistent with prior emotion regulation research using image-based stimuli, left prefrontal activity was observed during the implementation of all three strategies. Second, activity in a network of regions involved in self-referential processing and emotion, including subgenual anterior cingulate cortex and medial prefrontal cortex, was highest in response to the feel strategy and lowest for the accept strategy. This pattern of activation mirrored participants' self-reports of negative affect when engaging in each strategy.Conclusions These findings shed light on the brain regions that distinguish adaptive versus maladaptive forms of reflecting on negative autobiographical memories and offer a novel, ecologically valid route to exploring the neural bases of emotion regulation using fMRI.
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“Also, increased activity in areas associated with perspective taking predicted lower negative affect when decentering relative to the comparison condition – this included the superior parietal lobule, caudate and medial frontal gyrus.”
From Decentering as a core component in the psychological treatment and prevention of youth anxiety and depression: a narrative review and insight report (2021) · cites this paper as [45]
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“Findings suggest lower activity in areas associated with (intrapersonal) cognitive conflict and affective processing when decentering from negative memories relative to a comparison condition in which no attempt was made to alter ones experiences – brain regions included the medial and ventrolateral prefrontal cortex as well as the subgenual anterior cingulate45.”
From Decentering as a core component in the psychological treatment and prevention of youth anxiety and depression: a narrative review and insight report (2021) · cites this paper as [45]
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“there is some suggestion that acceptance may facilitate self-distancing and reappraisal of negative autobiographical memories, corresponding with comparative decreases in subgenual ACC and medial PFC activity (Kross, Davidson, Weber, & Ochsner, 2009).”
From Mechanisms of mindfulness training: Monitor and Acceptance Theory (MAT (2017) · cites this paper as Kross, Davidson, Weber, & Ochsner, 2009
In the citing paper
“activity within the subgenual cortex positively correlates with negative affect in healthy subjects (56–58)”
From Functional anatomy of ventromedial prefrontal cortex: implications for mood and anxiety disorders (2012) · cites this paper as [56]
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“Participants provided these cue phrases before the day of fMRI scanning using a procedure developed in prior research64”
From Separate neural representations for physical pain and social rejection (2014) · cites this paper as [64]
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“Collectively, these findings demonstrate that the benefits associated with distanced-analysis are neither a function of experimenter demand nor of cognitive avoidance (for discussion, see Ayduk & Kross, 2009; Kross & Ayduk, 2008).”
InfluentialSelf-citationBennett, M. P., Knight, R., Patel, S., So, T., Dunning, D., Barnhofer, T., Smith, P., Kuyken, W., Ford, T., & Dalgleish, T. (2021) · Translational Psychiatry · doi:10.1038/s41398-021-01397-5 · Cited by 81
Cognitive Vulnerability to Major Depression
Wang, X., Öngür, D., Auerbach, R. P., & Yao, S. (2016) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000081 · Cited by 96
“Similarly, Kross 75 reported that rumination induction in healthy subjects activated a network that included the subgenual ACC and medial PFC, and that this network activity was greater during induced rumination than during “ analyze ” or “ accept ” conditions.”
BackgroundRybnicek, R., Bergner, S., & Gutschelhofer, A. (2017) · Review of Managerial Science · doi:10.1007/s11846-017-0252-1 · Cited by 133
“In addition, the middle occipital gyrus is activated when emotions associated with autobiographical memories are regulated (Kross et al. 2009) or when rewards of high value are expected (e.g. Marsh et al. 2007).”
BackgroundAffective neuroscience of self‐generated thought
Fox, K. C. R., Andrews‐Hanna, J. R., Mills, C., Dixon, M. L., Markovic, J., Thompson, E. T., & Kalina Christoff, A. (2018) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13740 · Cited by 101
Zilles, K., Bacha‐Trams, M., Palomero‐Gallagher, N., Amunts, K., & Friederici, A. D. (2014) · Cortex · doi:10.1016/j.cortex.2014.07.007 · Cited by 88
Messina, I., Grecucci, A., & Viviani, R. (2021) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsab007 · Cited by 84
“Example of these instructions was ‘to focus on the specific feelings’ (Kross et al., 2009) or ‘become completely absorbed by feeling’ (Lebois et al., 2015).”
BackgroundResultInfluentialIs a Responsive Default Mode Network Required for Successful Working Memory Task Performance?
Čeko, M., Gracely, J. L., Fitzcharles, M., Seminowicz, D. A., Schweinhardt, P., & Bushnell, M. C. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0264-15.2015 · Cited by 75
“…(modulation of fMRI activity by increasing task load) in DMN regions and pain coping. fMRI activity in DMN regions has been linked to rumination (Kross et al., 2009) and specifically to increased rumination and catastrophizing about pain in patients with chronic pain (Kucyi et al., 2014), so we…”
BackgroundEmotion Regulation in Social Anxiety Disorder: Reappraisal and Acceptance of Negative Self-beliefs
Dixon, M. L., Moodie, C. A., Goldin, P. R., Farb, N. A. S., Heimberg, R. G., & Gross, J. J. (2019) · Biological Psychiatry Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.07.009 · Cited by 75
“Prior work has similarly found that DMN activation is lower during acceptance-based task conditions than comparison conditions (31,57).”
Morin, A., & Hamper, B. (2012) · The Open Neuroimaging Journal · doi:10.2174/1874440001206010078 · Cited by 80
“[141] Recalling AM of negative episodes in response to visual cues YES”
BackgroundFinding positive meaning in memories of negative events adaptively updates memory
Speer, M. E., Ibrahim, S., Schiller, D., & Delgado, M. R. (2021) · Nature Communications · doi:10.1038/s41467-021-26906-4 · Cited by 81
Weiss, J. A. (2014) · Clinical Psychology: Science and Practice · doi:10.1111/cpsp.12084 · Cited by 73
Neural correlates of recognition memory for emotional faces and scenes
Keightley, M., Chiew, K. S., Anderson, J. A. E., & Grady, C. L. (2010) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsq003 · Cited by 78
“The magnitude of emotion associated with autobiographical memories also influences activity in the amygdala and frontal cortex (Daselaar et al., 2008; Kross et al., 2009) and hippocampus (Addis et al., 2004) when these memories are retrieved.”
BackgroundFunctional connectivity of reflective and brooding rumination in depressed and healthy women
Satyshur, M. D., Layden, E. A., Gowins, J. R., Buchanan, A., & Gollan, J. K. (2018) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-018-0611-7 · Cited by 75
Tian, X. S., Wei, D., Du, X., Wang, K., Yang, J., Liu, W., Meng, J., Liu, H., Liu, G., & Qiu, J. (2016) · NeuroImage · doi:10.1016/j.neuroimage.2016.03.024 · Cited by 73
“…and the ALFF and ReHo in the right vmPFC were consistent with previous studies describing a role of the right vmPFC in the negative affect of individuals (Kross et al., 2009; Lemogne et al., 2012; Zald et al., 2002) and this associations were also observed in anxiety disorder (Shang et al., 2014).”
ResultGuo, C. C., Nguyen, V. T., Hyett, M. P., Parker, G. B., & Breakspear, M. J. (2015) · Scientific Reports · doi:10.1038/srep11605 · Cited by 74
Lois, G., & Wessa, M. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw085 · Cited by 66
“Rumination-induction has been associated with increased DMN functional connectivity (FC) and hyperactivity in MDD patients (Lemogne et al., 2009; Cooney et al., 2010; Kessler et al., 2011; Berman et al., 2014) and healthy subjects (Kross et al., 2009; Freton et al., 2014).”
BackgroundKross, E. F. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2009.04545.x · Cited by 68
Self-citationOrvell, A., Vickers, B. D., Drake, B., Verduyn, P., Ayduk, O., Moser, J., Jonides, J., & Kross, E. (2021) · Clinical Psychological Science · doi:10.1177/2167702620951539 · Cited by 63
Self-citationFerdek, M. A., van Rijn, C. M., & Wyczesany, M. (2016) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/s13415-016-0456-x · Cited by 67
Daubenmier, J., Hayden, D., Chang, V., & Epel, E. (2014) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2014.05.012 · Cited by 62
The neural component-process architecture of endogenously generated emotion
Engen, H. G., Kanske, P., & Singer, T. (2016) · Social Cognitive and Affective Neuroscience · doi:10.1093/scan/nsw108 · Cited by 59
“Plausibly, however, the opposite could be true, such that generation involves setting up representations of emotional situations, which in turn elicit core affective states (Kross et al., 2009).”
BackgroundNeural and behavioral correlates of negative self‐focused thought associated with depression
Philippi, C. L., Cornejo, M. D., Frost, C. P., Walsh, E. C., Hoks, R. M., Birn, R., & Abercrombie, H. C. (2018) · Human Brain Mapping · doi:10.1002/hbm.24003 · Cited by 60
“Similar to findings in MDD, neuroimaging studies in healthy individuals indicate that negative-SFT, such as rumination, is also associated with increased mPFC and ACC activity (e.g., Kross, Davidson, Weber, & Ochsner, 2009; Wagner et al., 2013) and connectivity (Berman et al., 2011).”
ResultEndogenous testosterone and cortisol modulate neural responses during induced anger control
Denson, T. F., Ronay, R., von Hippel, W., & Schira, M. M. (2012) · Social Neuroscience · doi:10.1080/17470919.2012.655425 · Cited by 65
“In such designs, blocks typically range in length from 30 s (e.g., Kross et al., 2009) to 110 s (e.g., Visscher et al., 2003).”
BackgroundNook, E. C., Satpute, A. B., & Ochsner, K. N. (2021) · Affective Science · doi:10.1007/s42761-021-00036-y · Cited by 82
Self-citationAbnormal prefrontal cortical response during affective processing in borderline personality disorder
Ruocco, A. C., Medaglia, J. D., Ayaz, H., & Chute, D. L. (2010) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2010.01.011 · Cited by 64
“The effortful regulation of negative affect appears to activate a distributed network of structures which includes areas of the frontal cortex (orbitofrontal and dorsomedial PFC), anterior cingulate, and amygdala (Levesque et al., 2003; Phan et al., 2005; Banks et al., 2007; Goldin et al., 2008; Kross et al., 2008).”
BackgroundMiller, B., & Sprang, G. (2017) · Traumatology · doi:10.1037/trm0000058 · Cited by 60
“As Levine (1997) has suggested, in humans, trauma may occur as a result of the initiation of the instinctual cycle that is not allowed to finish.”
BackgroundWang, K., Wei, D., Yang, J., Xie, P., Hao, X., & Qiu, J. (2015) · Psychological Medicine · doi:10.1017/s0033291715000938 · Cited by 61
“…medial and left superior frontal gyri, bilateral inferior frontal gyrus (IFG), right anterior cingulate cortex (ACC), left parahippocampal gyrus (PHG), left caudate, left inferior parietal lobe and amygdala (Putnam & McSweeney, 2008; Denson et al. 2009; Kross et al. 2009; Hooker et al. 2010).”
BackgroundResultAbend, R., Sar-El, R., Gonen, T., Jalon, I., Vaisvaser, S., Bar‐Haim, Y., & Hendler, T. (2018) · Neuromodulation Technology at the Neural Interface · doi:10.1111/ner.12787 · Cited by 55
Convergent Neural Correlates of Empathy and Anxiety During Socioemotional Processing
Knight, L. K., Stoica, T., Fogleman, N. D., & Depue, B. E. (2019) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2019.00094 · Cited by 63
The Neural Correlates of Cognitive Reappraisal during Emotional Autobiographical Memory Recall
Holland, A. C., & Kensinger, E. A. (2012) · Journal of Cognitive Neuroscience · doi:10.1162/jocn_a_00289 · Cited by 55
“However, reappraisal did not lead to any greater connectivity during the recall of angry AMs (Fabiansson et al., 2012), and it only led to increased activity in a region of left pFC that also was activated during rumination on sad AMs (Kross et al., 2009).”
BackgroundResultInfluentialNon-invasive vagal nerve stimulation decreases brain activity during trauma scripts
Wittbrodt, M. T., Gurel, N. Z., Nye, J. A., Ladd, S. L., Shandhi, M. M. H., Huang, M., Shah, A. J., Pearce, B. D., Alam, Z. S., Rapaport, M. H., et al. (2020) · Brain stimulation · doi:10.1016/j.brs.2020.07.002 · Cited by 56
“recall [72] and is likely involved in appraisal of the emotional state [69], and is functionally 308”
BackgroundRubin-Falcone, H., Weber, J., Kishon, R., Ochsner, K., Delaparte, L., Doré, B., Zanderigo, F., Oquendo, M. A., Mann, J. J., & Miller, J. M. (2018) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2017.11.002 · Cited by 53
“study (Kross et al., 2009), a region of interest (ROI) analysis was performed.”
InfluentialSelf-citationCortical abnormalities and association with symptom dimensions across the depressive spectrum
Lener, M. S., Kundu, P., Wong, E. W., DeWilde, K. E., Tang, C. Y., Balchandani, P., & Murrough, J. W. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.10.027 · Cited by 57
“For example, fMRI studies measuring neural activity in response to the induction of rumination have shown hyperactivity in the subgenual anterior cingulate cortex (sgACC) and dorso-medial prefrontal cortex (dmPFC) (Kross et al., 2009; Lemogne et al., 2009; Yoshimura et al., 2010), and hypoactivity in the dorsomedial t…”
Abnormal brain activation during directed forgetting of negative memory in depressed patients
Yang, W., Chen, Q., Liu, P., Cheng, H., Cui, Q., Wei, D., Zhang, Q., & Qiu, J. (2015) · Journal of Affective Disorders · doi:10.1016/j.jad.2015.05.034 · Cited by 55
“Previous neuroimaging studies also revealed that depressed individuals had reduced gray matter volumes in the MFG, bilateral IFG, SFG, left IPG, right anterior cingulate cortex, and left parahippocampal gyrus (Denson et al., 2009; Hooker et al., 2010; Kross et al., 2009; Putnam and McSweeney, 2008).”
BackgroundInhibitory control of emotional processing: Theoretical and empirical considerations
Bartholomew, M. E., Heller, W., & Miller, G. A. (2019) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2019.03.015 · Cited by 55
Autobiographical memory in depression: An fMRI study
Whalley, M. G., Rugg, M. D., & Brewin, C. R. (2012) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2011.08.008 · Cited by 55
“A study investigating emotional regulation strategies during retrieval of autobiographical memories found that a similar region of the left IFG (xyz [MNI]: −51 29 19) acted to implement a range of reappraisal operations (Kross et al., 2009).”
Guo, C. C., Hyett, M. P., Nguyen, V. T., Parker, G. B., & Breakspear, M. J. (2016) · Psychological Medicine · doi:10.1017/s0033291716000179 · Cited by 45
“In particular, subgenual ACC (sACC) and vmPFC are frequently reported to present altered activation and functional connectivity in depression (Drevets et al. 1997; Zald et al. 2002; Greicius et al. 2007; Kross et al. 2009; Walter et al. 2009; Myers-Schulz & Koenigs, 2012).”
Background
Metadata
- Authors
- Kross, E., Davidson, M., Weber, J., & Ochsner, K.
- Affiliations
- University of Michigan (US)
- Columbia University (US)
- Corresponding author
- Kross, Ethan
- Venue
- Biological Psychiatry
- Publisher
- Elsevier BV
- Published
- 2009-03
- Volume
- 65
- Issue
- 5
- Pages
- 361-366
- ISSN
- 0006-3223 (ISSN-L)
- PMC
- PMC2726992
- OpenAlex
- W2158177648
- Cited by
- 295
- References
- 40
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 15 · 2023: 17 · 2022: 17 · 2021: 15 · 2020: 11 · 2019: 15 · 2018: 20 · 2017: 19 · 2016: 22 · 2015: 24 · 2014: 24 · 2013: 28 · 2012: 17
- FWCI
- 5.68
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biological Psychiatry (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institute of Mental Health (R01MH076137, MH076137)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
- Social Sciences › Psychology › Developmental and Educational Psychology › Identity, Memory, and Therapy
- Keywords
- emotion regulation, rumination, self-referential processing, subgenual anterior cingulate cortex, medial prefrontal cortex, left prefrontal cortex, negative affect, cognitive strategies
- MeSH terms
- Adaptation, Psychological, Affect, Brain Mapping, Cognition, Emotions, Female, Gyrus Cinguli, Humans, Magnetic Resonance Imaging, Male, Memory, Prefrontal Cortex, Young Adult
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