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Article

Temporal Matching Between Interoception and Exteroception

Electrophysiological Responses in a Heartbeat Discrimination Task

Published Online:https://doi.org/10.1027/0269-8803/a000224

Abstract. Recent studies on interoception emphasize the importance of multisensory integration between interoception and exteroception. One of the methods frequently applied for assessing interoceptive sensitivity is the heartbeat discrimination task, where individuals judge whether the timing of external stimuli (e.g., tones) are synchronized to their own heartbeat. Despite its extensive use in research, the neural dynamics underlying the temporal matching between interoceptive and exteroceptive stimuli in this task have remained unclear. The present study used electroencephalography (EEG) to examine the neural responses of healthy participants who performed a heartbeat discrimination task. We analyzed the differences between EEG responses to tones, which were likely to be perceived as “heartbeat-synchronous” (200 ms delayed from the R wave) or “heartbeat-asynchronous” (0 ms delayed). Possible associations of these neural differentiations with task performance were also investigated. Compared with the responses to heartbeat-asynchronous tones, heartbeat-synchronous tones caused a relative decrease in early gamma-band EEG response and an increase in later P2 event-related potential (ERP) amplitude. Condition differences in the EEG/ERP measures were not significantly correlated with the behavioral measures. The mechanisms underlying the observed neural responses and the possibility of electrophysiological measurement of interoceptive sensitivity are discussed in terms of two perspectives: the predictive coding framework and the cardiac-phase-dependent baroreceptor function.

References

  • Aaronson, D. & Watts, B. (1987). Extensions of Grier’s computational formulas for A′ and B″ to below-chance performance. Psychological Bulletin, 102, 439–442. https://doi.org/10.1037/0033-2909.102.3.439 First citation in articleCrossrefGoogle Scholar

  • Acosta, A. & Pegalajar, J. (2003). Facilitation of heartbeat self-detection in a choice task. International Journal of Psychophysiology, 47, 139–146. https://doi.org/10.1016/S0167-8760(02)00121-6 First citation in articleCrossrefGoogle Scholar

  • Aronson, K. R., Barrett, L. F. & Quigley, K. (2006). Emotional reactivity and the overreport of somatic symptoms: Somatic sensitivity or negative reporting style? Journal of Psychosomatic Research, 60, 521–530. https://doi.org/10.1016/J.JPSYCHORES.2005.09.001 First citation in articleCrossrefGoogle Scholar

  • Apps, M. A. J. & Tsakiris, M. (2014). The free-energy self: A predictive coding account of self-recognition. Neuroscience & Biobehavioral Reviews, 41, 85–97. https://doi.org/10.1016/j.neubiorev.2013.01.029 First citation in articleCrossrefGoogle Scholar

  • Aspell, J. E., Heydrich, L., Marillier, G., Lavanchy, T., Herbelin, B. & Blanke, O. (2013). Turning body and self inside out: Visualized heartbeats alter bodily self-consciousness and tactile perception. Psychological Science, 24, 2445–2453. https://doi.org/10.1177/0956797613498395 First citation in articleCrossrefGoogle Scholar

  • Barrett, L. F., Quigley, K. S., Bliss-Moreau, E. & Aronson, K. R. (2004). Interoceptive sensitivity and self-reports of emotional experience. Journal of Personality and Social Psychology, 87, 684–697. https://doi.org/10.1037/0022-3514.87.5.684 First citation in articleCrossrefGoogle Scholar

  • Barrett, L. F. & Simmons, W. K. (2015). Interoceptive predictions in the brain. Nature Reviews Neuroscience, 16, 419–429. https://doi.org/10.1038/nrn3950 First citation in articleCrossrefGoogle Scholar

  • Başar, E. (2013). A review of gamma oscillations in healthy subjects and in cognitive impairment. International Journal of Psychophysiology, 90, 99–117. https://doi.org/10.1016/J.IJPSYCHO.2013.07.005 First citation in articleCrossrefGoogle Scholar

  • Benjamini, Y. & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57, 289–300. https://doi.org/10.2307/2346101 First citation in articleCrossrefGoogle Scholar

  • Blakemore, S. J., Goodbody, S. J. & Wolpert, D. M. (1998). Predicting the consequences of our own actions: The role of sensorimotor context estimation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 18, 7511–7518. https://doi.org/10.1523/JNEUROSCI.18-18-07511.1998 First citation in articleCrossrefGoogle Scholar

  • Blanke, O., Slater, M. & Serino, A. (2015). Behavioral, neural, and computational principles of bodily self-consciousness. Neuron, 88, 145–166. https://doi.org/10.1016/j.neuron.2015.09.029 First citation in articleCrossrefGoogle Scholar

  • Brener, J. & Ring, C. (2016). Towards a psychophysics of interoceptive processes: The measurement of heartbeat detection. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20160015. https://doi.org/10.1098/rstb.2016.0015 First citation in articleCrossrefGoogle Scholar

  • Brown, H., Adams, R. A., Parees, I., Edwards, M. & Friston, K. (2013). Active inference, sensory attenuation and illusions. Cognitive Processing, 14, 411–427. https://doi.org/10.1007/s10339-013-0571-3 First citation in articleCrossrefGoogle Scholar

  • Cameron, O. G. (2001). Interoception: The inside story – A model for psychosomatic processes. Psychosomatic Medicine, 63, 697–710. https://doi.org/10.1097/00006842-200109000-00001 First citation in articleCrossrefGoogle Scholar

  • Clark, A. (2013). Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behavioral and Brain Sciences, 36, 181–204. https://doi.org/10.1017/S0140525X12000477 First citation in articleCrossrefGoogle Scholar

  • Cohen, M. X. (2014). Analyzing neural time series data: Theory and practice. Cambridge, MA: MIT Press. First citation in articleCrossrefGoogle Scholar

  • Craig, A. D. (2009). How do you feel – now? The anterior insula and human awareness. Nature Reviews. Neuroscience, 10, 59–70. https://doi.org/10.1038/nrn2555 First citation in articleCrossrefGoogle Scholar

  • Critchley, H. D. & Garfinkel, S. N. (2015). Interactions between visceral afferent signaling and stimulus processing. Frontiers in Neuroscience, 9, 286. https://doi.org/10.3389/fnins.2015.00286 First citation in articleCrossrefGoogle Scholar

  • Critchley, H. D. & Garfinkel, S. N. (2017). Interoception and emotion. Current Opinion in Psychology, 17, 7–14. https://doi.org/10.1016/j.copsyc.2017.04.020 First citation in articleCrossrefGoogle Scholar

  • Critchley, H. D., Wiens, S., Rotshtein, P., Ohman, A. & Dolan, R. J. (2004). Neural systems supporting interoceptive awareness. Nature Neuroscience, 7, 189–195. https://doi.org/10.1038/nn1176 First citation in articleCrossrefGoogle Scholar

  • Davis, M. R., Langer, A. W., Sutterer, J. R., Gelling, P. D. & Marlin, M. (1986). Relative discriminability of heartbeat-contingent stimuli under three procedures for assessing cardiac perception. Psychophysiology, 23, 76–81. https://doi.org/10.1111/j.1469-8986.1986.tb00598.x First citation in articleCrossrefGoogle Scholar

  • Domschke, K., Stevens, S., Pfleiderer, B. & Gerlach, A. L. (2010). Interoceptive sensitivity in anxiety and anxiety disorders: An overview and integration of neurobiological findings. Clinical Psychology Review, 30, 1–11. https://doi.org/10.1016/j.cpr.2009.08.008 First citation in articleCrossrefGoogle Scholar

  • Dunn, B. D., Galton, H. C., Morgan, R., Evans, D., Oliver, C., Meyer, M., … Dalgleish, T. (2010). Listening to your heart. How interoception shapes emotion experience and intuitive decision making. Psychological Science, 21, 1835–1844. https://doi.org/10.1177/0956797610389191 First citation in articleCrossrefGoogle Scholar

  • Duschek, S., Werner, N. S. & Reyes del Paso, G. A. (2013). The behavioral impact of baroreflex function: A review. Psychophysiology, 50, 1183–1193. https://doi.org/10.1111/psyp.12136 First citation in articleCrossrefGoogle Scholar

  • Dworkin, B. R., Elbert, T., Rau, H., Birbaumer, N., Pauli, P., Droste, C. & Brunia, C. H. (1994). Central effects of baroreceptor activation in humans: Attenuation of skeletal reflexes and pain perception. Proceedings of the National Academy of Sciences of the United States of America, 91, 6329–6333. https://doi.org/10.1073/pnas.91.14.6329 First citation in articleCrossrefGoogle Scholar

  • Edwards, L., McIntyre, D., Carroll, D., Ring, C. & Martin, U. (2002). The human nociceptive flexion reflex threshold is higher during systole than diastole. Psychophysiology, 39, 678–681. https://doi.org/10.1111/1469-8986.3950678 First citation in articleCrossrefGoogle Scholar

  • Edwards, L., Ring, C., McIntyre, D., Winer, J. B. & Martin, U. (2009). Sensory detection thresholds are modulated across the cardiac cycle: Evidence that cutaneous sensibility is greatest for systolic stimulation. Psychophysiology, 46, 252–256. https://doi.org/10.1111/j.1469-8986.2008.00769.x First citation in articleCrossrefGoogle Scholar

  • Friston, K. (2009). The free-energy principle: A rough guide to the brain? Trends in Cognitive Sciences, 13, 293–301. https://doi.org/10.1016/j.tics.2009.04.005 First citation in articleCrossrefGoogle Scholar

  • Gandal, M. J., Edgar, J. C., Ehrlichman, R. S., Mehta, M., Roberts, T. P. L. & Siegel, S. J. (2010). Validating γ oscillations and delayed auditory responses as translational biomarkers of autism. Biological Psychiatry, 68, 1100–1106. https://doi.org/10.1016/j.biopsych.2010.09.031 First citation in articleCrossrefGoogle Scholar

  • Garfinkel, S. N. & Critchley, H. D. (2016). Threat and the body: How the heart supports fear processing. Trends in Cognitive Sciences, 20, 34–46. https://doi.org/10.1016/j.tics.2015.10.005 First citation in articleCrossrefGoogle Scholar

  • Garfinkel, S. N., Minati, L., Gray, M. A, Seth, A. K., Dolan, R. J. & Critchley, H. D. (2014). Fear from the heart: Sensitivity to fear stimuli depends on individual heartbeats. The Journal of Neuroscience, 34, 6573–6582. https://doi.org/10.1523/JNEUROSCI.3507-13.2014 First citation in articleCrossrefGoogle Scholar

  • Garfinkel, S. N., Seth, A. K., Barrett, A. B., Suzuki, K. & Critchley, H. D. (2015). Knowing your own heart: Distinguishing interoceptive accuracy from interoceptive awareness. Biological Psychology, 104, 65–74. https://doi.org/10.1016/j.biopsycho.2014.11.004 First citation in articleCrossrefGoogle Scholar

  • Garrido, M. I., Kilner, J. M., Kiebel, S. J. & Friston, K. J. (2007). Evoked brain responses are generated by feedback loops. Proceedings of the National Academy of Sciences of the United States of America, 104, 20961–20966. https://doi.org/10.1073/pnas.0706274105 First citation in articleCrossrefGoogle Scholar

  • Gray, M. A., Beacher, F. D., Minati, L., Nagai, Y., Kemp, A. H., Harrison, N. A. & Critchley, H. D. (2012). Emotional appraisal is influenced by cardiac afferent information. Emotion, 12, 180–191. https://doi.org/10.1037/a0025083 First citation in articleCrossrefGoogle Scholar

  • Grier, J. B. (1971). Nonparametric indexes for sensitivity and bias: Computing formulas. Psychological Bulletin, 75, 424–429. https://doi.org/10.1037/h0031246 First citation in articleCrossrefGoogle Scholar

  • Hantas, M. N., Katkin, E. S. & Reed, S. D. (1984). Cerebral lateralization and heartbeat discrimination. Psychophysiology, 21, 274–278. https://doi.org/10.1111/j.1469-8986.1984.tb02934.x First citation in articleCrossrefGoogle Scholar

  • Harver, A., Katkin, E. S. & Bloch, E. (1993). Signal-detection outcomes on heartbeat and respiratory resistance detection tasks in male and female subjects. Psychophysiology, 30, 223–230. https://doi.org/10.1111/j.1469-8986.1993.tb03347.x First citation in articleCrossrefGoogle Scholar

  • Hegerl, U., Gallinat, J. & Mrowinski, D. (1994). Intensity dependence of auditory evoked dipole source activity. International Journal of Psychophysiology, 17, 1–13. https://doi.org/10.1016/0167-8760(94)90050-7 First citation in articleCrossrefGoogle Scholar

  • Herbert, B. M., Herbert, C. & Pollatos, O. (2011). On the relationship between interoceptive awareness and alexithymia: Is interoceptive awareness related to emotional awareness? Journal of Personality, 79, 1149–1175. https://doi.org/10.1111/j.1467-6494.2011.00717.x First citation in articleCrossrefGoogle Scholar

  • Herbert, B. M. & Pollatos, O. (2012). The body in the mind: On the relationship between interoception and embodiment. Topics in Cognitive Science, 4, 692–704. First citation in articleCrossrefGoogle Scholar

  • Herbert, B. M., Pollatos, O. & Schandry, R. (2007). Interoceptive sensitivity and emotion processing: An EEG study. International Journal of Psychophysiology, 65, 214–227. https://doi.org/10.1016/j.ijpsycho.2007.04.007 First citation in articleCrossrefGoogle Scholar

  • Hughes, G., Desantis, A. & Waszak, F. (2013). Mechanisms of intentional binding and sensory attenuation: The role of temporal prediction, temporal control, identity prediction, and motor prediction. Psychological Bulletin, 139, 133–151. https://doi.org/10.1037/a0028566 First citation in articleCrossrefGoogle Scholar

  • Jones, G. E. (1994). Perception of visceral sensations: A review of recent findings, methodologies, and future directions. In J. R. JenningsP. K. AcklesM. G. H. ColesEds., Advances in psychophysiology: A research annual (Vol. 5, pp. 55–191). London, UK: Jessica Kingsley. First citation in articleGoogle Scholar

  • Karakaş, S. & Başar, E. (1998). Early gamma response is sensory in origin: A conclusion based on cross-comparison of results from multiple experimental paradigms. International Journal of Psychophysiology, 31, 13–31. https://doi.org/10.1016/S0167-8760(98)00030-0 First citation in articleCrossrefGoogle Scholar

  • Katkin, E. S., Blascovich, J. & Goldband, S. (1981). Empirical assessment of visceral self-perception: Individual and sex differences in the acquisition of heartbeat discrimination. Journal of Personality and Social Psychology, 40, 1095–1101. https://doi.org/10.1037/0022-3514.40.6.1095 First citation in articleCrossrefGoogle Scholar

  • Key, A. P. F., Dove, G. O. & Maguire, M. J. (2005). Linking brainwaves to the brain: An ERP primer. Developmental Neuropsychology, 27, 183–215. https://doi.org/10.1207/s15326942dn2702_1 First citation in articleCrossrefGoogle Scholar

  • Khalsa, S. S., Rudrauf, D., Damasio, A. R., Davidson, R. J., Lutz, A. & Tranel, D. (2008). Interoceptive awareness in experienced meditators. Psychophysiology, 45, 671–677. https://doi.org/10.1111/j.1469-8986.2008.00666.x First citation in articleCrossrefGoogle Scholar

  • Lamme, V. A. F. & Roelfsema, P. R. (2000). The distinct modes of vision offered by feedforward and recurrent processing. Trends in Neurosciences, 23, 571–579. https://doi.org/10.1016/S0166-2236(00)01657-X First citation in articleCrossrefGoogle Scholar

  • La Rovere, M. T., Pinna, G. D. & Raczak, G. (2008). Baroreflex sensitivity: Measurement and clinical implications. Annals of Noninvasive Electrocardiology, 13, 191–207. https://doi.org/10.1111/j.1542-474X.2008.00219.x First citation in articleCrossrefGoogle Scholar

  • Martins, A. Q., Ring, C., McIntyre, D., Edwards, L. & Martin, U. (2009). Effects of unpredictable stimulation on pain and nociception across the cardiac cycle. Pain, 147, 84–90. https://doi.org/10.1016/j.pain.2009.08.016 First citation in articleCrossrefGoogle Scholar

  • McIntyre, D., Edwards, L., Ring, C., Parvin, B. & Carroll, D. (2006). Systolic inhibition of nociceptive responding is moderated by arousal. Psychophysiology, 43, 314–319. https://doi.org/10.1111/j.1469-8986.2006.00407.x First citation in articleCrossrefGoogle Scholar

  • McIntyre, D., Kavussanu, M. & Ring, C. (2008). Effects of arterial and cardiopulmonary baroreceptor activation on the upper limb nociceptive flexion reflex and electrocutaneous pain in humans. Pain, 137, 550–555. https://doi.org/10.1016/j.pain.2007.10.018 First citation in articleCrossrefGoogle Scholar

  • Merwin, R. M., Zucker, N. L., Lacy, J. L. & Elliott, C. A. (2010). Interoceptive awareness in eating disorders: Distinguishing lack of clarity from non-acceptance of internal experience. Cognition & Emotion, 24, 892–902. https://doi.org/10.1080/02699930902985845 First citation in articleCrossrefGoogle Scholar

  • Pantev, C., Makeig, S., Hoke, M., Galambos, R., Hampson, S. & Gallen, C. (1991). Human auditory evoked gamma-band magnetic fields. Proceedings of the National Academy of Sciences of the United States of America, 88, 8996–9000. https://doi.org/10.1073/pnas.88.20.8996 First citation in articleCrossrefGoogle Scholar

  • Park, H.-D., Correia, S., Ducorps, A. & Tallon-Baudry, C. (2014). Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nature Neuroscience, 17, 612–618. https://doi.org/10.1038/nn.3671 First citation in articleCrossrefGoogle Scholar

  • Pennebaker, J. W. (1981). Stimulus characteristics influencing estimation of heart rate. Psychophysiology, 18, 540–548. https://doi.org/10.1111/j.1469-8986.1981.tb01824.x First citation in articleCrossrefGoogle Scholar

  • Pennebaker, J. W. & Roberts, T.-A. (1992). Toward a his and hers theory of emotion: Gender differences in visceral perception. Journal of Social and Clinical Psychology, 11, 199–212. First citation in articleCrossrefGoogle Scholar

  • Phillips, G. C., Jones, G. E., Rieger, E. J. & Snell, J. B. (1999). Effects of the presentation of false heart-rate feedback on the performance of two common heartbeat-detection tasks. Psychophysiology, 36, 504–510. https://doi.org/10.1017/S0048577299980071 First citation in articleCrossrefGoogle Scholar

  • Ponton, C. W., Eggermont, J. J., Kwong, B. & Don, M. (2000). Maturation of human central auditory system activity: Evidence from multi-channel evoked potentials. Clinical Neurophysiology, 111, 220–236. https://doi.org/10.1016/S1388-2457(99)00236-9 First citation in articleCrossrefGoogle Scholar

  • Quattrocki, E. & Friston, K. (2014). Autism, oxytocin and interoception. Neuroscience & Biobehavioral Reviews, 47, 410–430. https://doi.org/10.1016/j.neubiorev.2014.09.012 First citation in articleCrossrefGoogle Scholar

  • Ring, C. & Brener, J. (1992). The temporal locations of heartbeat sensations. Psychophysiology, 29, 535–545. https://doi.org/10.1111/j.1469-8986.1992.tb02027.x First citation in articleCrossrefGoogle Scholar

  • Ring, C. & Brener, J. (1996). Influence of beliefs about heart rate and actual heart rate on heartbeat counting. Psychophysiology, 33, 541–546. https://doi.org/10.1111/j.1469-8986.1996.tb02430.x First citation in articleCrossrefGoogle Scholar

  • Ring, C., Brener, J., Knapp, K. & Mailloux, J. (2015). Effects of heartbeat feedback on beliefs about heart rate and heartbeat counting: A cautionary tale about interoceptive awareness. Biological Psychology, 104, 193–198. https://doi.org/10.1016/j.biopsycho.2014.12.010 First citation in articleCrossrefGoogle Scholar

  • Salomon, R., Ronchi, R., Dönz, J., Bello-Ruiz, J., Herbelin, B., Martet, R., … Blanke, O. (2016). The insula mediates access to awareness of visual stimuli presented synchronously to the heartbeat. Journal of Neuroscience, 36, 5115–5127. https://doi.org/10.1523/JNEUROSCI.4262-15.2016 First citation in articleCrossrefGoogle Scholar

  • Sandercock, G. R. H., Bromley, P. D. & Brodie, D. A. (2005). The reliability of short-term measurements of heart rate variability. International Journal of Cardiology, 103, 238–247. https://doi.org/10.1016/j.ijcard.2004.09.013 First citation in articleCrossrefGoogle Scholar

  • Schandry, R. (1981). Heart beat perception and emotional experience. Psychophysiology, 18, 483–488. https://doi.org/10.1111/j.1469-8986.1981.tb02486.x First citation in articleCrossrefGoogle Scholar

  • Schulz, A., Lass-Hennemann, J., Nees, F., Blumenthal, T. D., Berger, W. & Schachinger, H. (2009). Cardiac modulation of startle eye blink. Psychophysiology, 46, 234–240. https://doi.org/10.1111/j.1469-8986.2008.00768.x First citation in articleCrossrefGoogle Scholar

  • Schulz, A., Lass-Hennemann, J., Sütterlin, S., Schächinger, H. & Vögele, C. (2013). Cold pressor stress induces opposite effects on cardioceptive accuracy dependent on assessment paradigm. Biological Psychology, 93, 167–174. https://doi.org/10.1016/j.biopsycho.2013.01.007 First citation in articleCrossrefGoogle Scholar

  • Sel, A., Azevedo, R. T. & Tsakiris, M. (2016). Heartfelt self: Cardio-visual integration affects self-face recognition and interoceptive cortical processing. Cerebral Cortex, 27, 573–582. https://doi.org/10.1093/cercor/bhw296 First citation in articleGoogle Scholar

  • Seth, A. K. (2013). Interoceptive inference, emotion, and the embodied self. Trends in Cognitive Sciences, 17, 565–573. https://doi.org/10.1016/j.tics.2013.09.007 First citation in articleCrossrefGoogle Scholar

  • Shah, P., Hall, R., Catmur, C. & Bird, G. (2016). Alexithymia, not autism, is associated with impaired interoception. Cortex, 81, 215–220. https://doi.org/10.1016/J.CORTEX.2016.03.021 First citation in articleCrossrefGoogle Scholar

  • Sueyoshi, T., Sugimoto, F., Katayama, J. & Fukushima, H. (2014). Neural correlates of error processing reflect individual differences in interoceptive sensitivity. International Journal of Psychophysiology, 94, 278–286. https://doi.org/10.1016/j.ijpsycho.2014.10.001 First citation in articleCrossrefGoogle Scholar

  • Suzuki, K., Garfinkel, S. N., Critchley, H. D. & Seth, A. K. (2013). Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion. Neuropsychologia, 51, 2909–2917. https://doi.org/10.1016/j.neuropsychologia.2013.08.014 First citation in articleCrossrefGoogle Scholar

  • Terasawa, Y., Shibata, M., Moriguchi, Y. & Umeda, S. (2013). Anterior insular cortex mediates bodily sensibility and social anxiety. Social Cognitive and Affective Neuroscience, 8, 259–266. https://doi.org/10.1093/scan/nss108 First citation in articleCrossrefGoogle Scholar

  • Terhaar, J., Viola, F. C., Bär, K.-J. & Debener, S. (2012). Heartbeat evoked potentials mirror altered body perception in depressed patients. Clinical Neurophysiology, 123, 1950–1957. https://doi.org/10.1016/j.clinph.2012.02.086 First citation in articleCrossrefGoogle Scholar

  • van Elk, M., Lenggenhager, B., Heydrich, L. & Blanke, O. (2014). Suppression of the auditory N1-component for heartbeat-related sounds reflects interoceptive predictive coding. Biological Psychology, 99, 172–182. https://doi.org/10.1016/j.biopsycho.2014.03.004 First citation in articleCrossrefGoogle Scholar

  • Vaughan, H. G. & Ritter, W. (1970). The sources of auditory evoked responses recorded from the human scalp. Electroencephalography and Clinical Neurophysiology, 28, 360–367. https://doi.org/10.1016/0013-4694(70)90228-2 First citation in articleCrossrefGoogle Scholar

  • von Holst, E. (1954). Relations between the central Nervous System and the peripheral organs. The British Journal of Animal Behaviour, 2, 89–94. https://doi.org/10.1016/S0950-5601(54)80044-X First citation in articleCrossrefGoogle Scholar

  • Wiens, S., Mezzacappa, E. S. & Katkin, E. S. (2000). Heartbeat detection and the experience of emotions. Cognition & Emotion, 14, 417–427. https://doi.org/10.1080/026999300378905 First citation in articleCrossrefGoogle Scholar

  • Wiens, S. & Palmer, S. N. (2001). Quadratic trend analysis and heartbeat detection. Biological Psychology, 58, 159–175. https://doi.org/10.1016/S0301-0511(01)00110-7 First citation in articleCrossrefGoogle Scholar

  • Wittmann, M. (2015). Modulations of the experience of self and time. Consciousness and Cognition, 38, 172–181. https://doi.org/10.1016/j.concog.2015.06.008 First citation in articleCrossrefGoogle Scholar

  • Wolpert, D. M. (1997). Computational approaches to motor control. Trends in Cognitive Sciences, 1, 209–216. https://doi.org/10.1016/S1364-6613(97)01070-X First citation in articleCrossrefGoogle Scholar