Resting heart rate variability is associated with inhibition of conditioned fear
Abstract
Startle blink as well as skin conductance responses (SCR) are widely used indices of learning processes associated with fear conditioning and extinction. During safety learning, the amygdala is under top-down inhibitory control by the prefrontal cortex (PFC). The capacity of the PFC to exert inhibitory control over subcortical brain structures may be indexed by resting state vagally mediated heart rate variability (HRV). The present study investigated the association of resting HRV with startle blink and SCR during conditioned fear inhibition and extinction. Participants first learned to discriminate a threat cue (A) signaling an aversive unconditioned stimulus from a safety signal (B), which were each presented together with a third stimulus X (AX+/BX-). Then, both the threat and safety signal were presented together (AB) to test whether the presence of the learned safety signal inhibits the fear response to the danger signal. Finally, AX was presented without reinforcement (AX-) to investigate fear extinction. Higher HRV was associated with pronounced fear inhibition and fear extinction. Resting HRV levels were associated with fear extinction as indexed by startle blink potentiation but not SCR, which presumably reflect more cognitive aspects of learning. Resting HRV may reflect the capacity of the prefrontal cortex to inhibit subcortical fear responses in the presence of safety or when former threat cues are presented in the absence of threat.
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Not recognizing safety is not restricted to people suffering from stressors or anxiety.
“Moreover, not recognizing safety is not restricted to people suffering from stressors or anxiety (Pappens et al., 2014;Ruiz-Padial et al., 2003;Wendt et al., 2015).”
From Exposed to events that never happen: generalized unsafety, the default stress response, and prolonged autonomic activity (2017) · cites this paper as Wendt et al., 2015
Cites
An Integrative Theory of Prefrontal Cortex Function
Miller, E. K., & Cohen, J. D. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.167 · Cited by 12,803 · see citing works
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J., & Wager, T. D. (2012) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2011.11.009 · Cited by 3,224 · see citing works
Self-citationA model of neurovisceral integration in emotion regulation and dysregulation
Thayer, J. F., & Lane, R. D. (2000) · Journal of Affective Disorders · doi:10.1016/s0165-0327(00)00338-4 · Cited by 3,092 · see citing works
Self-citationThayer, J. F., & Lane, R. D. (2009) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2008.08.004 · Cited by 2,040 · see citing works
Self-citationThayer, J. F., Hansen, A. L., Saus-Rose, E., & Johnsen, B. H. (2009) · Annals of Behavioral Medicine · doi:10.1007/s12160-009-9101-z · Cited by 1,872 · see citing works
Self-citationContext and Behavioral Processes in Extinction: Table 1.
Bouton, M. E. (2004) · Learning & Memory · doi:10.1101/lm.78804 · Cited by 1,808 · see citing works
Myers, K. M., & Davis, M. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4001939 · Cited by 1,277 · see citing works
Fear and anxiety: Animal models and human cognitive psychophysiology
Lang, P. J., Davis, M., & Öhman, A. (2000) · Journal of Affective Disorders · doi:10.1016/s0165-0327(00)00343-8 · Cited by 1,162 · see citing works
Anxiety Disorders are Associated with Reduced Heart Rate Variability: A Meta-Analysis
Chalmers, J. A., Quintana, D. S., Abbott, M. J.-A., & Kemp, A. H. (2014) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2014.00080 · Cited by 1,067 · see citing works
DIRECT MEASUREMENT OF SKIN CONDUCTANCE: A PROPOSAL FOR STANDARDIZATION
Lykken, D. T., & Venables, P. H. (1971) · Psychophysiology · doi:10.1111/j.1469-8986.1971.tb00501.x · Cited by 988 · see citing works
Quirk, G. J., Likhtik, E., Pelletier, J. G., & Paré, D. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-25-08800.2003 · Cited by 927 · see citing works
Software for advanced HRV analysis
Niskanen, J., Tarvainen, M. P., Ranta-aho, P. O., & Karjalainen, P. A. (2004) · Computer Methods and Programs in Biomedicine · doi:10.1016/j.cmpb.2004.03.004 · Cited by 789 · see citing works
The role of awareness in Pavlovian conditioning: empirical evidence and theoretical implications.
Lovibond, P., & Shanks, D. (2002) · Journal of experimental psychology. Animal behavior processes · doi:10.1037/0097-7403.28.1.3 · Cited by 748 · see citing works
Prefrontal mechanisms in extinction of conditioned fear
Quirk, G. J., Garcia, R., & González-Lima, F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.03.010 · Cited by 682 · see citing works
Impaired safety signal learning may be a biomarker of PTSD
Jovanovic, T., Kazama, A., Bachevalier, J., & Davis, M. (2012) · Neuropharmacology · doi:10.1016/j.neuropharm.2011.02.023 · Cited by 473 · see citing works
The role of the amygdala in fear-potentiated startle: implications for animal models of anxiety
Davis, M. (1992) · Trends in Pharmacological Sciences · doi:10.1016/0165-6147(92)90014-w · Cited by 427 · see citing works
Anatomic-histological Description of the Birds' Singing Larynx
Pavlov, L. T. (1927) · Acta Oto-Laryngologica · doi:10.3109/00016482709120085 · Cited by 368 · see citing works
The neuropsychology of fear learning and fear regulation
Hamm, A. O., & Weike, A. I. (2005) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2005.01.006 · Cited by 290 · see citing works
Self-citationAffective learning: Awareness and aversion
HAMM, A. O., & VAITL, D. (1996) · Psychophysiology · doi:10.1111/j.1469-8986.1996.tb02366.x · Cited by 282 · see citing works
Self-citationLyonfields, J. D., Borkovec, T. D., & Thayer, J. F. (1995) · Behavior Therapy · doi:10.1016/s0005-7894(05)80094-2 · Cited by 247 · see citing works
Self-citationLissek, S., Rabin, S. J., McDowell, D. J., Dvir, S., Bradford, D. E., Geraci, M., Pine, D. S., & Grillon, C. (2009) · Behaviour Research and Therapy · doi:10.1016/j.brat.2008.10.017 · Cited by 239 · see citing works
Heart rate and heart rate variability changes in the intracarotid sodium amobarbital test
Ahern, G. L., Sollers, J. J., Lane, R. D., Labiner, D. M., Herring, A. M., Weinand, M. E., Hutzler, R., & Thayer, J. F. (2001) · Epilepsia · doi:10.1046/j.1528-1157.2001.042007912.x · Cited by 195 · see citing works
Affective blindsight: intact fear conditioning to a visual cue in a cortically blind patient
Hamm, A. O. (2003) · Brain · doi:10.1093/brain/awg037 · Cited by 181 · see citing works
Self-citationRuiz‐Padial, E., Sollers, J. J., Vila, J., & Thayer, J. F. (2003) · Psychophysiology · doi:10.1111/1469-8986.00032 · Cited by 179 · see citing works
Self-citationFear acquisition requires awareness in trace but not delay conditioning
Weike, A. I., Schupp, H. T., & Hamm, A. O. (2007) · Psychophysiology · doi:10.1111/j.1469-8986.2006.00469.x · Cited by 163 · see citing works
Self-citationFear potentiation and fear inhibition in a human fear-potentiated startle paradigm
Jovanovic, T., Keyes, M., Fiallos, A., Myers, K. M., Davis, M., & Duncan, E. J. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.02.025 · Cited by 150 · see citing works
Neural correlates of giving support to a loved one
Inagaki, T. K., & Eisenberger, N. I. (2012) · Psychosomatic Medicine · doi:10.1097/psy.0b013e3182359335 · Cited by 141 · see citing works
Melzig, C. A., Weike, A. I., Hamm, A. O., & Thayer, J. F. (2009) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2008.07.013 · Cited by 126 · see citing works
Craske, M. G., Wolitzky-Taylor, K. B., Mineka, S., Zinbarg, R., Waters, A. M., Vrshek-Schallhorn, S., Epstein, A., Naliboff, B., & Ornitz, E. (2012) · Journal of Abnormal Psychology · doi:10.1037/a0025738 · Cited by 112 · see citing works
Cardiac vagal tone is correlated with selective attention to neutral distractors under load
Park, G., Vasey, M. W., Bavel, J. J. V., & Thayer, J. F. (2013) · Psychophysiology · doi:10.1111/psyp.12029 · Cited by 96 · see citing works
Self-citationGillie, B. L., & Thayer, J. F. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00758 · Cited by 92 · see citing works
Self-citationPappens, M., Schroijen, M., Sütterlin, S., Smets, E., Van den Bergh, O., Thayer, J. F., & Van Diest, I. (2014) · PLoS ONE · doi:10.1371/journal.pone.0105054 · Cited by 91 · see citing works
Sevenster, D., Beckers, T., & Kindt, M. (2012) · Psychophysiology · doi:10.1111/j.1469-8986.2012.01450.x · Cited by 88 · see citing works
Dawson, M. E., Schell, A. M., & Banis, H. T. (1986) · Psychophysiology · doi:10.1111/j.1469-8986.1986.tb00673.x · Cited by 88 · see citing works
Myers, K. M., & Davis, M. E. (2004) · Learning & Memory · doi:10.1101/lm.74704 · Cited by 87 · see citing works
Lindner, K., Neubert, J., Pfannmöller, J. P., Lotze, M., Hamm, A. O., & Wendt, J. (2015) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2015.02.025 · Cited by 86 · see citing works
Self-citationKrypotos, A., Jahfari, S., van Ast, V. A., Kindt, M., & Forstmann, B. U. (2011) · Frontiers in Psychology · doi:10.3389/fpsyg.2011.00278 · Cited by 73 · see citing works
Luck, C. C., & Lipp, O. V. (2015) · Behaviour Research and Therapy · doi:10.1016/j.brat.2015.01.001 · Cited by 58 · see citing works
Psychophysiological Response Patterns to Affective Film Stimuli
Bos, M. G. N., Jentgens, P., Beckers, T., & Kindt, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062661 · Cited by 54 · see citing works
On the resistance to extinction of fear conditioned to angry faces.
Rowles, M. E., Lipp, O., & Mallan, K. (2012) · Psychophysiology · doi:10.1111/j.1469-8986.2011.01308.x · Cited by 44 · see citing works
Genetic influences on the acquisition and inhibition of fear
Wendt, J., Neubert, J., Lindner, K., Ernst, F. D., Homuth, G., Weike, A. I., & Hamm, A. O. (2014) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2014.10.007 · Cited by 34 · see citing works
Self-citationResting heart rate variability and the startle reflex to briefly presented affective pictures
Ruiz‐Padial, E., & Thayer, J. F. (2014) · International Journal of Psychophysiology · doi:10.1016/j.ijpsycho.2014.10.005 · Cited by 24 · see citing works
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Brosschot, J. F., Verkuil, B., & Thayer, J. F. (2017) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.07.019 · Cited by 178 · see citing works
Self-citationDi Bello, M., Carnevali, L., Petrocchi, N., Thayer, J. F., Gilbert, P., & Ottaviani, C. (2020) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2020.06.016 · Cited by 154 · see citing works
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Clamor, A., Koenig, J., Thayer, J. F., & Lincoln, T. M. (2016) · Behaviour Research and Therapy · doi:10.1016/j.brat.2016.10.003 · Cited by 40 · see citing works
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- Authors
- Wendt, J., Neubert, J., Koenig, J., Thayer, J. F., & Hamm, A. O.
- Affiliations
- Universität Greifswald (DE)
- Heidelberg University (DE)
- The Ohio State University (US)
- Corresponding author
- Wendt, Julia
- Venue
- Psychophysiology
- Publisher
- Wiley
- Published
- 2015-06-11
- Volume
- 52
- Issue
- 9
- Pages
- 1161-1166
- ISSN
- 0048-5772 (ISSN-L)
- 1469-8986
- OpenAlex
- W2164051630
- Cited by
- 85
- References
- 42
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 9 · 2023: 7 · 2022: 12 · 2021: 8 · 2020: 8 · 2019: 10 · 2018: 6 · 2017: 8 · 2016: 7 · 2015: 1
- FWCI
- 4.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Psychophysiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- German Research Society (DFG) (WE 2762/5-1)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Neurology › Vagus Nerve Stimulation Research
- Keywords
- resting heart rate variability, fear extinction, fear inhibition, skin conductance response, safety learning, prefrontal cortex, top-down inhibition, amygdala, vagal tone, threat cues
- MeSH terms
- Adult, Blinking, Conditioning, Psychological, Electrocardiography, Extinction, Psychological, Fear, Female, Heart Rate, Humans, Inhibition, Psychological, Male, Reinforcement, Psychology, Reflex, Startle, Young Adult
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