What the heart forgets: cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity
Open accessAbstract
Mental functions are influenced by states of physiological arousal. Afferent neural activity from arterial baroreceptors at systole conveys the strength and timing of individual heartbeats to the brain. We presented words under limited attentional resources time‐locked to different phases of the cardiac cycle, to test a hypothesis that natural baroreceptor stimulation influences detection and subsequent memory of words. We show memory for words presented around systole was decreased relative to words at diastole. The deleterious memory effect of systole was greater for words detected with low confidence and amplified in individuals with low interoceptive sensitivity, as indexed using a heartbeat counting task. Our observations highlight an important cardiovascular channel through which autonomic arousal impacts a cognitive function, an effect mitigated by metacognition (perceptual confidence) and interoceptive sensitivity.
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The dimensional model of interoception can be extended further to incorporate lower level measures of afferent neural traffic and the preconscious impact of interoceptive signals on sensory processing.
“This dimensional model of interoception can be extended further to incorporate lower level measures of afferent neural traffic (quantifying afferent signal strength, e.g. through heartbeat evoked potentials [20 ]), and the preconscious impact of interoceptive signals on sensory processing (e.g.modification of startle response [21 ,22] or augmentation of threat processing [23 ,24,25]).”
From Interoception and emotion. (2017) · cites this paper as [22]
The paper’s background passage (section labelled Abstract; page unavailable) describes cardiac afferent signals and their effects on perceptual processing, and its Discussion reports an effect of cardiac timing on later word memory. It does not establish the claimed extension of a dimensional model or measure afferent signal strength with heartbeat-evoked potentials; its Results also found no cardiac-timing effect on word detection. The cited paper therefore supports the broader idea that interoceptive signals can affect processing, but not the full claim attributed to it. (LLM, conf=0.82)
Experimental — accuracy not yet measuredWord recognition memory is modulated by the timing of visual stimuli with respect to cardiac phase under restricted attention.
“For example, word recognition memory is modulated by the timing of visual stimuli with respect to cardiac phase under restricted attention [63].”
From Interoceptive inference, emotion, and the embodied self (2013) · cites this paper as [63]
Short-term respiratory afferent signals, like cardiac afferent signals, modify defensive reflexes (notably startle responses) and nasopharyngeal airflow influences processing of affective information.
“Short-term respiratory afferent signals, like cardiac afferent signals, modify defensive reflexes (notably startle responses [22]) and even nasopharyngeal airflow (an internal, yet mostly exteroceptive, respiratory stimulus) also influences processing of affective information [28 ].”
From Interoception and emotion. (2017) · cites this paper as [22]
Citation [22] is attached to the claim about defensive reflexes, notably startle responses; the nasopharyngeal-airflow claim has a separate citation. The paper's introductory passage discusses cardiac timing and the processing of somatosensory stimuli, pain, and emotional faces, while its Discussion reports effects on word memory. Searches for startle and defensive reflexes found no passage addressing those responses. (LLM, conf=0.77)
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Critchley, H. D., & Garfinkel, S. N. (2018) · Current Opinion in Behavioral Sciences · doi:10.1016/j.cobeha.2017.08.014 · Cited by 178 · see citing works
Self-citationCardiac afferent activity modulates the expression of racial stereotypes
Azevedo, R. T., Garfinkel, S. N., Critchley, H. D., & Tsakiris, M. (2017) · Nature Communications · doi:10.1038/ncomms13854 · Cited by 133 · see citing works
Self-citationEmotion, somatovisceral afference, and autonomic regulation
Norman, G. J., Berntson, G. G., & Cacioppo, J. T. (2014) · Emotion Review · doi:10.1177/1754073913512006 · Cited by 97 · see citing works
Mind-Body Interactions in Anxiety and Somatic Symptoms
Mallorquí-Bagué, N., Bulbena, A., Pailhez, G., Garfinkel, S. N., & Critchley, H. D. (2016) · Harvard Review of Psychiatry · doi:10.1097/hrp.0000000000000085 · Cited by 96 · see citing works
Self-citationResponse inhibition on the stop signal task improves during cardiac contraction
Rae, C. L., Botan, V. E., Gould van Praag, C. D., Herman, A. M., Nyyssönen, J. A. K., Watson, D. R., Duka, T., Garfinkel, S. N., & Critchley, H. D. (2018) · Scientific Reports · doi:10.1038/s41598-018-27513-y · Cited by 83 · see citing works
Self-citationActive information sampling varies across the cardiac cycle
Kunzendorf, S., Klotzsche, F., Akbal, M., Villringer, A., Ohl, S., & Gaebler, M. (2019) · Psychophysiology · doi:10.1111/psyp.13322 · Cited by 73 · see citing works
Effect of Parasympathetic Stimulation on Brain Activity During Appraisal of Fearful Expressions
Makovac, E., Garfinkel, S. N., Bassi, A., Basile, B., Macaluso, E., Cercignani, M., Calcagnini, G., Mattei, E., Agalliu, D., Cortelli, P., et al. (2015) · Neuropsychopharmacology · doi:10.1038/npp.2015.10 · Cited by 54 · see citing works
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Barttfeld, P., Wicker, B., McAleer, P., Belin, P., Cojan, Y., Graziano, M., Leiguarda, R., & Sigman, M. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1301353110 · Cited by 41 · see citing works
The Relationship Between Interoception and Metacognition: A Pilot Study
Meessen, J., Mainz, V., Gauggel, S., Volz-Sidiropoulou, E., Sütterlin, S., & Forkmann, T. (2016) · Journal of Psychophysiology · doi:10.1027/0269-8803/a000157 · Cited by 37 · see citing works
Relationship between cardiac cycle and the timing of actions during action execution and observation
Palser, E. R., Glass, J., Fotopoulou, A., & Kilner, J. M. (2021) · Cognition · doi:10.1016/j.cognition.2021.104907 · Cited by 37 · see citing works
Feeling in Control: The Role of Cardiac Timing in the Sense of Agency
Herman, A. M., & Tsakiris, M. (2020) · Affective Science · doi:10.1007/s42761-020-00013-x · Cited by 37 · see citing works
Abrevaya, S., Fittipaldi, S., García, A. M., Dottori, M., Santamaria-Garcia, H., Birba, A., Yoris, A., Hildebrandt, M. K., Salamone, P., De la Fuente, A., et al. (2020) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000868 · Cited by 34 · see citing works
Rhesus monkeys have an interoceptive sense of their beating hearts
Charbonneau, J. A., Maister, L., Tsakiris, M., & Bliss-Moreau, E. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2119868119 · Cited by 35 · see citing works
- Authors
- Garfinkel, S. N., Barrett, A. B., Minati, L., Dolan, R. J., Seth, A. K., & Critchley, H. D.
- Affiliations
- Brighton and Sussex Medical School (GB)
- University of Sussex (GB)
- Wellcome Centre for Human Neuroimaging (GB)
- Corresponding author
- Garfinkel, Sarah N.
- ORCID
- Venue
- Psychophysiology
- Publisher
- Wiley
- Published
- 2013-03-22
- Volume
- 50
- Issue
- 6
- Pages
- 505-512
- ISSN
- 0048-5772 (ISSN-L)
- 1469-8986
- PMC
- PMC4340570
- OpenAlex
- W2125572598
- Semantic Scholar
- c08265d15a2d736ee1c67f0a14018a984961ceac
- Cited by
- 176
- References
- 80
- Citations by year
- 2026: 10 · 2025: 16 · 2024: 18 · 2023: 12 · 2022: 9 · 2021: 13 · 2020: 14 · 2019: 13 · 2018: 16 · 2017: 18 · 2016: 17 · 2015: 8 · 2014: 9 · 2013: 3
- FWCI
- 8.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Psychophysiology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion, other-oa)
- Figshare (submittedVersion, cc-by)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Sussex Research Online (University of Sussex) (submittedVersion)
- Funders
- Wellcome Trust (091593, 098362, 098362/Z/12/Z)
- European Commission (258749)
- Engineering and Physical Sciences Research Council (EP/G007543/1)
- FP7 Information and Communication Technologies
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- baroreceptors, systole, diastole, word memory, metacognition, interoceptive sensitivity, heartbeat counting, autonomic arousal, physiological arousal, perceptual confidence, attentional resources
- MeSH terms
- Adult, Arousal, Attention, Autonomic Nervous System, Cognition, Emotions, Female, Heart, Heart Rate, Humans, Male, Memory, Psychomotor Performance, Self Concept, Systole, Young Adult
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