Skip to main content
SpringerLink
Log in

Interoception and embodiment in patients with bilateral vestibulopathy

  • Original Communication
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

There are tight functional and anatomical links between the vestibular and interoceptive systems, and both systems have shown to fundamentally underlie emotional processes and our sense of a bodily self. Yet, nothing is known about how long-term bilateral vestibulopathy (BVP) influences interoception and its relation to embodiment and the sense of self. We thus compared cardiac interoceptive accuracy, confidence in the performance, and general body awareness in 25 BVP patients and healthy controls using a heartbeat tracking task, self-reports about interoceptive awareness, as well as measures of self-localization and of self–body closeness. Results showed no difference between patients and controls regarding interoceptive accuracy, confidence and body awareness, suggesting that long-term BVP does not influence cardiac interoception. Patients and controls did not differ either regarding self-location and self–body closeness. However, in our overall sample of patients and controls, we found that interoceptive accuracy increased with perceived self–body closeness, suggesting that anchoring the self to the body is generally linked with better cardiac interoception. This result is in line with previous suggestions of an important contribution of interoception to the sense of embodiment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Smith PF (2017) The vestibular system and cognition. Curr Opin Neurol 30:84–89. https://doi.org/10.1097/WCO.0000000000000403

    Article  PubMed  Google Scholar 

  2. Lopez C (2016) The vestibular system: balancing more than just the body. Curr Opin Neurol 29:74–83. https://doi.org/10.1097/WCO.0000000000000286

    Article  PubMed  Google Scholar 

  3. Jauregui-Renaud K (2015) Vestibular function and depersonalization/derealization symptoms. Multisens Res 28:637–651

    Article  Google Scholar 

  4. Jacob RG, Furman JM (2001) Psychiatric consequences of vestibular dysfunction. Curr Opin Neurol 14:41–46

    Article  CAS  Google Scholar 

  5. Lucieer F, Duijn S, Van Rompaey V et al (2018) Full spectrum of reported symptoms of bilateral vestibulopathy needs further investigation—a systematic review. Front Neurol. https://doi.org/10.3389/fneur.2018.00352

    Article  PubMed  PubMed Central  Google Scholar 

  6. Craig AD (2003) Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13:500–505

    Article  CAS  Google Scholar 

  7. Khalsa SS, Adolphs R, Cameron OG et al (2018) Interoception and Mental Health: a roadmap. Biol Psychiatry CognNeurosci Neuroimaging 3:501–513. https://doi.org/10.1016/j.bpsc.2017.12.004

    Article  Google Scholar 

  8. Blanke O (2012) Multisensory brain mechanisms of bodily self-consciousness. Nat Rev Neurosci 13:556–571. https://doi.org/10.1038/nrn3292

    Article  PubMed  CAS  Google Scholar 

  9. Azzalini D, Rebollo I, Tallon-Baudry C (2019) Visceral signals shape brain dynamics and cognition. Trends Cogn Sci 23:488–509. https://doi.org/10.1016/j.tics.2019.03.007

    Article  PubMed  Google Scholar 

  10. Park H-D, Blanke O (2019) Coupling inner and outer body for self-consciousness. Trends Cogn Sci 23:377–388. https://doi.org/10.1016/j.tics.2019.02.002

    Article  PubMed  Google Scholar 

  11. Craig AD (2009) How do youfeel-now? The anterior insula and humanawareness. Nat Rev Neurosci 10:59–70. https://doi.org/10.1038/nrn2555

    Article  PubMed  CAS  Google Scholar 

  12. Dutov AM (1974) Responses of neurons of the vestibular nuclei to interoceptive stimulation. Bull Exp Biol Med 78:849–851

    Article  Google Scholar 

  13. Balaban CD, Porter JD (1998) Neuroanatomic substrates for vestibulo-autonomic interactions. J Vestib Res 8:7–16

    PubMed  CAS  Google Scholar 

  14. Jauregui-Renaud K, Gresty MA, Reynolds R, Bronstein AM (2001) Respiratory responses of normal and vestibular defective human subjects to rotation in the yaw and pitch planes. Neurosci Lett 298:17–20. https://doi.org/10.1016/S0304-3940(00)01731-6

    Article  PubMed  CAS  Google Scholar 

  15. Schandry R (1981) Heart beat perception and emotional experience. Psychophysiology 18:483–488

    Article  CAS  Google Scholar 

  16. Garfinkel SN, Seth AK, Barrett AB et al (2015) Knowing your own heart: distinguishing interoceptive accuracy from interoceptive awareness. Biol Psychol 104:65–74. https://doi.org/10.1016/j.biopsycho.2014.11.004

    Article  PubMed  Google Scholar 

  17. Frasnelli J, Collignon O, Voss P, Lepore F (2011) Crossmodal plasticity in sensory loss. Prog Brain Res 191:233–249. https://doi.org/10.1016/B978-0-444-53752-2.00002-3

    Article  PubMed  Google Scholar 

  18. Beaulieu-Lefebvre M, Schneider FC, Kupers R, Ptito M (2011) Odor perception and odor awareness in congenital blindness. Brain Res Bull 84:206–209. https://doi.org/10.1016/j.brainresbull.2010.12.014

    Article  PubMed  Google Scholar 

  19. Mittelstaedt H (1992) Somatic versus vestibular gravity reception in man. Ann N Y Acad Sci 656:124–139

    Article  CAS  Google Scholar 

  20. Krajnik J, Kollndorfer K, Notter LA et al (2015) The impact of olfactory dysfunction on interoceptive awareness. Psychophysiology 52:263–268. https://doi.org/10.1111/psyp.12316

    Article  PubMed  Google Scholar 

  21. Montoya P, Schandry R (1994) Emotional experience and heartbeat perception in patients with spinal cord injury and control subjects. J Psychophysiol 8:289–296

    Google Scholar 

  22. Cabrera A, Kolacz J, Pailhez G et al (2018) Assessing body awareness and autonomic reactivity: factor structure and psychometric properties of the Body Perception Questionnaire-Short Form (BPQ-SF). Int J Methods Psychiatr Res 27:e1596. https://doi.org/10.1002/mpr.1596

    Article  PubMed  Google Scholar 

  23. Critchley HD, Wiens S, Rotshtein P et al (2004) Neural systems supporting interoceptive awareness. Nat Neurosci 7:189–195

    Article  CAS  Google Scholar 

  24. Starmans C, Bloom P (2012) Windows to the soul: Children and adults see the eyes as the location of the self. Cognition 123:313–318. https://doi.org/10.1016/j.cognition.2012.02.002

    Article  PubMed  Google Scholar 

  25. Limanowski J, Hecht H (2011) Where do we stand on locating the self? Psychology 02:312–317. https://doi.org/10.4236/psych.2011.24049

    Article  Google Scholar 

  26. Fetterman AK, Robinson MD (2013) Do you use your head or follow your heart? Self-location predicts personality, emotion, decision making, and performance. J Pers Soc Psychol 105:316–334. https://doi.org/10.1037/a0033374

    Article  PubMed  PubMed Central  Google Scholar 

  27. Porciello G, Daum MM, Menghini C et al (2016) Not that heart-stopping after all: visuo-cardiac synchrony does not boost self-face attribution. PLoS ONE 11:e0160498. https://doi.org/10.1371/journal.pone.0160498

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Deroualle D, Toupet M, van Nechel C et al (2017) Anchoring the self to the body in bilateral vestibular failure. PLoS ONE 12:e0170488. https://doi.org/10.1371/journal.pone.0170488

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Strupp M, Arbusow V, Dieterich M et al (1998) Perceptual and oculomotor effects of neck muscle vibration in vestibular neuritis. Ipsilateral somatosensory substitution of vestibular function. Brain 121:677–685

    Article  Google Scholar 

  30. Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67:361–370

    Article  CAS  Google Scholar 

  31. Peirce JW (2007) PsychoPy—psychophysics software in python. J Neurosci Methods 162:8–13

    Article  Google Scholar 

  32. Aron A, Aron EN, Smollan D (1992) Inclusion of other in the self scale and the structure of interpersonal closeness. J Pers Soc Psychol 63:596–612. https://doi.org/10.1037/0022-3514.63.4.596

    Article  Google Scholar 

  33. Ring C, Brener J (2018) Heartbeat counting is unrelated to heartbeat detection: a comparison of methods to quantify interoception. Psychophysiology 55:e13084. https://doi.org/10.1111/psyp.13084

    Article  PubMed  Google Scholar 

  34. Jauregui-Renaud K, Yarrow K, Oliver R et al (2000) Effects of caloric stimulation on respiratory frequency and heart rate and blood pressure variability. Brain Res Bull 53:17–23. https://doi.org/10.1016/s0361-9230(00)00304-x

    Article  PubMed  CAS  Google Scholar 

  35. Garfinkel SN, Manassei MF, Hamilton-Fletcher G et al (2016) Interoceptive dimensions across cardiac and respiratory axes. Philos Trans R Soc Lond, B, Biol Sci. https://doi.org/10.1098/rstb.2016.0014

    Article  PubMed Central  Google Scholar 

  36. Trousselard M, Barraud P, Nougier V et al (2004) Contribution of tactile and interoceptive cues to the perception of the direction of gravity. Brain Res Cogn Brain Res 20:355–362. https://doi.org/10.1016/j.cogbrainres.2004.03.008

    Article  PubMed  Google Scholar 

  37. Lopez C, Nakul E, Preuss N et al (2018) Distorted own-body representations in patients with dizziness and during caloric vestibular stimulation. J Neurol 265:86–94. https://doi.org/10.1007/s00415-018-8906-8

    Article  PubMed  Google Scholar 

  38. Lopez C, Elzière M (2018) Out-of-body experience in vestibular disorders—a prospective study of 210 patients with dizziness. Cortex 104:193–206. https://doi.org/10.1016/j.cortex.2017.05.026

    Article  PubMed  Google Scholar 

  39. Ferrè ER, Lopez C, Haggard P (2014) Anchoring the self to the body: vestibular contribution to the sense of self. Psychol Sci 25:2106–2108. https://doi.org/10.1177/0956797614547917

    Article  PubMed  Google Scholar 

  40. Deroualle D, Borel L, Devèze A, Lopez C (2015) Changing perspective: the role of vestibularsignals. Neuropsychologia 79(Part B):175–185. https://doi.org/10.1016/j.neuropsychologia.2015.08.022

    Article  PubMed  Google Scholar 

  41. Candidi M, Micarelli A, Viziano A et al (2013) Impaired mental rotation in benign paroxysmal positional vertigo and acute vestibular neuritis. Front Hum Neurosci 7:783. https://doi.org/10.3389/fnhum.2013.00783

    Article  PubMed  PubMed Central  Google Scholar 

  42. Claparède E (1925) Note sur la localisation du moi. Arch Psychol 19:172–182

    Google Scholar 

  43. Tsakiris M, Tajadura-Jiménez A, Costantini M (2011) Just a heartbeat away from one’s body: interoceptive sensitivity predicts malleability of body-representations. Proc Biol Sci 278:2470–2476. https://doi.org/10.1098/rspb.2010.2547

    Article  PubMed  PubMed Central  Google Scholar 

  44. Tschan R, Wiltink J, Adler J et al (2013) Depersonalization experiences are strongly associated with dizziness and vertigo symptoms leading to increased health care consumption in the German general population. J NervMent Dis 201:629–635. https://doi.org/10.1097/NMD.0b013e3182982995

    Article  Google Scholar 

  45. Kolev OI, Georgieva-Zhostova SO, Berthoz A (2014) Anxiety changes depersonalization and derealization symptoms in vestibular patients. Behav Neurol 2014:847054. https://doi.org/10.1155/2014/847054

    Article  PubMed  PubMed Central  Google Scholar 

  46. Noel J-P, Pfeiffer C, Blanke O, Serino A (2015) Peripersonal space as the space of the bodily self. Cognition 144:49–57. https://doi.org/10.1016/j.cognition.2015.07.012

    Article  PubMed  PubMed Central  Google Scholar 

  47. Nakul E, Orlando-Dessaints N, Lenggenhager B, Lopez C (2020) Measuring perceived self-location in virtual reality. Sci Rep 10:6802. https://doi.org/10.1038/s41598-020-63643-y

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

The authors declare no competing financial interests. The research leading to these results has received funding from the Swiss National Science Foundation (Grant number: PP00P1_170511).

Author information

Author notes

  1. Bigna Lenggenhager and Christophe Lopez shared last authorship. These authors contributed equally to the present study.

Authors and Affiliations

  1. Aix Marseille Univ, CNRS, LNSC, Marseille, France

    Estelle Nakul, Charles Dabard & Christophe Lopez

  2. IRON, Institut de Recherche en Oto-Neurologie, Paris, France

    Michel Toupet, Charlotte Hautefort & Christian van Nechel

  3. Centre D’Explorations Fonctionnelles Oto-Neurologiques, Paris, France

    Michel Toupet

  4. Service ORL, Hôpital Lariboisière, Paris, France

    Charlotte Hautefort

  5. Unité Troubles de l’Équilibre et Vertiges, CHU Brugmann, Bruxelles, Belgium

    Christian van Nechel

  6. Unité de Neuro-Ophtalmologie, CHU Erasme, Bruxelles, Belgium

    Christian van Nechel

  7. Clinique des Vertiges, Bruxelles, Belgium

    Christian van Nechel

  8. Cognitive Neuropsychology, Department of Psychology, University of Zurich, Zurich, Switzerland

    Bigna Lenggenhager

Authors
  1. Estelle Nakul
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles Dabard
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michel Toupet
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Charlotte Hautefort
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christian van Nechel
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bigna Lenggenhager
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christophe Lopez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christophe Lopez.

Ethics declarations

Conflicts of interest

None.

Ethical approval

Procedures were approved by the Ethics Committee and followed the Declaration of Helsinki.

Informed consent

All participants were informed about the study and gave written informed consent.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nakul, E., Dabard, C., Toupet, M. et al. Interoception and embodiment in patients with bilateral vestibulopathy. J Neurol 267 (Suppl 1), 109–117 (2020). https://doi.org/10.1007/s00415-020-10221-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-020-10221-x

Keywords

Search

Navigation