The representation of heart contractions in some auditory parts of the temporal cortex in a non-anesthetized cat

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The inquiry into how cortical neurons respond to interoceptive signals remains a complex puzzle, central to understanding self-awareness in advanced mammals, including humans. A fundamental aspect under scrutiny is whether neural networks in the cerebral cortex of animals can accurately reflect internal bodily states, particularly cardiac activity. To investigate this, we conducted a study on neurons within the temporal cortex of awake and sleeping cat, employing a unique setup enabling continuous differential recording of local potentials in specific cortical regions, alongside monitoring the cardiogram. Our findings revealed intriguing insights. While the primary auditory cortex (AI) exhibited minimal cellular activity synchronized with heartbeats, the secondary auditory zones within the temporal cortex – the anterior ectosylvian sulcus and the posterior ectosylvian gyrus – displayed synchronization with heart rate. This synchronization was particularly evident in local potentials, with certain neurons within these zones responding to sounds and also exhibiting rhythmic activity aligned with heart contractions. Notably, the complexity of phase histograms derived from the cardiogram period suggests that this synchronization is not attributable to artifacts but rather represents genuine neural responses. Our observations prompt consideration of a hypothesis regarding primary self-awareness in both humans and animals. We propose that this phenomenon emerges from the dynamic interaction of two neural ensembles: one representing external sensory input and the other reflecting interoceptive signals, notably from the heart. This interplay between external and internal stimuli may underpin the fundamental experience of the consciousness of self in highly developed organisms.

作者简介

N. Bibikov

JSC N.N. Andreev Acoustic Institute; A.A. Kharkevich Institute of Information Transmission Problems of the Russian Academy of Sciences

编辑信件的主要联系方式.
Email: nbibikov1@yandex.ru
俄罗斯联邦, 4 Shvernik str., Moscow, 117036; 19 Bolshoy Karetny Lane, Moscow, 127051

I. Pigarev

A.A. Kharkevich Institute of Information Transmission Problems of the Russian Academy of Sciences

Email: nbibikov1@yandex.ru
俄罗斯联邦, 19 Bolshoy Karetny Lane, Moscow, 127051

参考

  1. Bibikov N. G., Nizamov S. V., Pigarev I. N. Neyronnyye reakzii kory mozga koshki na zvuki, postupayushchiye s frontal'nogo napravleniya (metodicheskiye aspekty) [Neural reactions of the cat's cerebral cortex to sounds coming from the frontal direction (methodological aspects)]. Trudy vserossiyskoy akusticheskoy konferentsii. Politekh-Press Sankt-Peterburg [Proceedings of the All-Russian Acoustic Conference. Polytechnic Press. St. Petersburg 2020]. 2020. P. 281–284. ISBN978–5–7422–7029–4.(in Russian).
  2. Lavrova V. D., Busygina I. I., Pigarev I. N. Otrazheniye serdechnoy aktivnosti v elektroentsefalogramme koshek v periody medlennogo sna u koshek [Reflection of heart activity in the electroencephalogram of cats during periods of slow sleep in cats]. Sensornye systemy. [Sensory systems]. 2019. V. 33. P. 70–76. URL: https://doi.10.1134/S0235009219010086 (in Russian).
  3. Musyashchikova S. S., Chernigovskiy V. N. Kortikal'noye i subkortikal'noye predstavitel'stvo vistseral'nykh system [Cortical and subcortical representation of visceral systems]. Leningrad: Nauka, 1973. 288 p. (in Russian).
  4. Pigarev I. N., Bibikov N. G. Issledovaniye obrabotki “slukhovykh” zon visochnoy kory mozga koshki v period sna v analize informatsii, postupayushchey ot vistseral'nykh organov [A study of the involvement of the “auditory” zones of the temporal cortex of the cat's brain during sleep in the analysis of information coming from visceral organs.]. Sbornik IX mezhdunarodnogo foruma “Son” 2022 [Proceedingsof the IX International forum “Sleep” 2022.]. Moscow: “Sam poligrafist”. 2022. P. 6. ISBN: 978–5–00166–638–7 (in Russian).
  5. Al E., Iliopoulos F., Nikulin V. V., Villringer A. Heartbeat and somatosensory perception. NeuroImage. 2021. V.238. Article 118247. URL: https://doi.org/10.1016/j.neuroimage
  6. Andrews-Hanna J.R., Smallwood J., Spreng R. N. The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Ann. N. Y. Acad. Sci. 2014. V. 1316. P. 29–52. URL: https://doi.10.1111/nyas.12360
  7. Andrews K., Birch J., Sebo J., Sims T. Background to the New York Declaration on Animal Consciousness. 2024. nydeclaration.com
  8. Arnau S., Sharifian F., Wascher E., Larra M. Removing the cardiac field artifact from the EEG using neural network regression. Psychophysiology. 2023. URL: https://doi./10.1111/psyp.14323
  9. Azzalini D., Rebollo I., Tallon-Baudry C. Visceral signals shape brain dynamics and cognition. Trends in Cognit. Sci. V. 23. P. 488–509. URL: https://doi./10.1016/j.tics.2019.03.007
  10. Babo-Rebelo M., Richter C. G., Tallon-Baudry C. Neural responses to heartbeats in the default network encode the self in spontaneous thoughts. J. Neurosci. 2016. V. 36. P. 7829–7840. URL: https://doi.10.1523/JNEUROSCI.0262–16.2016
  11. Babo-Rebelo M., Buot A., Tallon-Baudry C. Neural responses to heartbeats distinguish self from other during imagination. NeuroImage. 2019. V. 191. P. 10–20. URL: https://doi.10.1016/j.neuroimage.2019.02.012
  12. Bibikov N. G. Functional studies of the primary auditory cortex in the cat. Neurosci. Behav. Physiol. 2021. V. 51. P. 1169–1189. URL: https://doi.10.1007/s11055–021–01177–0
  13. Candia-Rivera D. Brain-heart interactions in the neurobiology of consciousness. Current Res. Neurobiol. 2022. V. 3. Article 100050. URL: https://doi.10.1016/j.crneur.2022.100050
  14. Chouchou F., Mauguière F., Vallayer O. et al. How the insula speaks to the heart: Cardiac responses to insular stimulation in humans. Human Brain Mapping. 2019. V. 40 (9). URL: https://doi.10.1002/hbm.24548
  15. Clarey J. C., Irvine D. R. The anterior ectosylviansulcal auditory field in the cat: I. An electrophysiological study of its relationship to surrounding auditory cortical fields. J. Comp. Neurol. 1990a. V. 301. P. 289–303. URL: https://doi: 10.1002/cne.903010211
  16. Clarey J. C., Irvine D. R. The anterior ectosylviansulcal auditory field in the cat: II. A horseradish peroxidase study of its thalamic and cortical connections. J. Comp. Neurol. 1990b. V. 301. P. 304–324. URL: https://doi.10.1002/cne.903010212
  17. Clarke E. L. Aristotelian concepts of the form and function of the brain. Bull.Hist Medicine. 1963. V. 37. P. 1–14.
  18. Coll M. P., Hobson H., Bird G., Murphy J. Systematic review and meta-analysis of the relationship between the heartbeat-evoked potential and interoception. Neurosci. Biobehav. Rev. 2021. V. 122. P. 190–200. URL: https://doi.10.1016/j.neubiorev.2020.12.012
  19. Dai C., Wang J., Xie J. et al. Removal of ECG artifacts from EEG using an effective recursive least square notch filter. IEEE Access. 2019. V. 7. P. 158872–158880. URL: https://doi.10.1109/access.2019.2949842
  20. Edelman D. B. Animal Consciousness. In: William P. Banks, (Editor), Encyclopedia of Consciousness. 2009. Oxford: Elsevier. V. 1. P. 23–36.
  21. Erisir A., Van Horn S. C., Sherman S. M. Relative numbers of cortical and brainstem inputs to the lateral geniculate nucleus. Proc. Nat. Acad. Sci. USA, 1997. V. 94 (4). P. 1517–1520. URL: https://doi.10.1073/pnas.94.4.1517
  22. Fitzpatrick D., Diamond I. T., Raczkowski D. Cholinergic and monoaminergic innervation of the cat's thalamus: comparison of the lateral geniculate nucleus with other principal sensory nuclei. J. Comp Neurol. 1989. V. 288. P. 647–675. URL: https://doi.10.1002/cne.902880411
  23. Frewen P., Northoff G., Riva G. et al. Neuroimaging the consciousness of self: review, and conceptual-methodological framework. Neurosci. Biobehav. Rev. 2020. V. 112. P. 164–212. URL: https://doi.10.1016/j.neubiorev.2020.01.023.
  24. Frysinger R., Harper R. Cardiac and respiratory relationships with neural discharge in the anterior cingulate cortex during sleep-waking states. Exp.Neurol. 1986. V. 94. P. 247–263. URL: https://doi.10.1016/0014–4886(86)90100–7
  25. Gray M. A., Taggart P., Sutton P. M. et al. A cortical potential reflecting cardiac function. Proc. Natl. Acad. Sci. U. S. A. 2007. V. 104. P. 6818–6823. URL: https://doi.10.1073/pnas.0609509104
  26. Gross C. G. Aristotle and the brain. Neuroscientist. 1995. V. 1. P. 245–250. URL: https://doi.10.1177/107385849500100408
  27. He J., Hashikawa T. Connections of the dorsal zone of cat auditory cortex. J. Comp. Neurol. 1998. V.400. P. 334–448. URL: https://doi. 10.1002/(sici)1096–9861(19981026)400:3<334:: aid-cne4>3.0.co;2–9
  28. Jiang H., Lepore F., Poirier P., Guillemot J. P. Responses of cells to stationary and moving sound stimuli in the anterior ectosylvian cortex of cats. Hear. Res. 2000. V. 139. P. 69–85. URL: https://doi.10.1016/s0378–5955(99)00176–8
  29. Kim K., Ladenbauer J., Babo-Rebelo M. et al. Resting-state neural firing rate is linked to cardiac-cycle duration in the human. J. Neurosci. 2019. V. 39. P. 3676–3686. URL: https://doi.10.1523/JNEUROSCI.2291–18.2019.
  30. Kok M. A., Stolzberg D., Brown T. A., Lomber S. G. Dissociable influences of primary auditory cortex and the posterior auditory field on neuronal responses in the dorsal zone of auditory cortex. J. Neurophysiol. 2015. V. 113. P. 475–486. URL: https://doi.10.1152/jn.00682.2014.
  31. Las L., Shapira A. H., Nelken I. Functional gradients of auditory sensitivity along the anteriorectosylvian sulcus of the cat. J. Neurosci. 2008. V. 28. P. 3657–3667. URL: https://doi.10.1523/JNEUROSCI.4539–07.2008
  32. Lechinger J., Heib D. P., Gruber W., Schabus M., Klimesch W. Heartbeat-related EEG amplitude and phase modulations from wakefulness to deep sleep: Interactions with sleep spindles and slow oscillations. Psychophysiol. 2015. V. 52(11). P. 1441–1450. URL: https://doi.10.1111/psyp.12508.
  33. Massimini M., Porta A., Mariotti M., Malliani A., Montano N. Heart rate variability is encoded in the spontaneous discharge of thalamic somatosensory neurones in cat. J. Physiol. 2000. V. 526. P. 387–396. doi: 10.1111/j.1469–7793.2000.t01–1–00387.x
  34. Mellott J. G., Van der Gucht E., Lee C. C. et al. Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32. Hear. Res. 2010. V. 267. P. 119–136. URL: https://doi.10.1016/j.heares.2010.04.003
  35. Meredith M. A., Clemo H. R. Auditory cortical projection from the anterior ectosylvian sulcus (Field AES) to the superior colliculus in the cat: an anatomical and electrophysiological study. J. Comp. Neurol. 1989. V. 289. P. 687–707. URL: https://doi.10.1002/cne.902890412
  36. Meredith M. A., Wallace M. T., Clemo H. R. Do the different sensory areas within the cat anterior ectosylviansulcal cortex collectively represent a network multisensory hub? Multisens. Res. 2018. V. 31(8). P. 793–823. URL: https://doi. 10.1163/22134808–20181316
  37. Oppenheimer S., Cechetto D. The insular cortex and the regulation of cardiac function. Comprehen. Physiol. 2016. V. 6. P. 1081–1133. URL: https://doi.10.1002/cphy.c140076
  38. Park H. D., Correia S., Ducorps A., Tallon-Baudry C. Spontaneous fluctuations in neural responses to heartbeats predict visual detection. Nat. Neurosci. 2014. V. 17. P. 612–618. URL: https://doi.10.1038/nn.3671
  39. Park H. D., Bernasconi F., Salomon R. et al. Neural sources and underlying mechanisms of neural responses to heartbeats, and their role in bodily self-consciousness: an intracranial EEG study. Cereb. Cortex. 2018. V. 28, P. 2351–2364. URL: https://doi.10.1093/cercor/bhx136
  40. Park H-D., Blanke O. Heartbeat-evoked cortical responses: Underlying mechanisms, functional roles, and methodological considerations. NeuroImage. 2019. V. 197. P. 502–511. URL: https://doi.10.1016/j.neuroimage.2019.04.081
  41. Perez J. J., Guijarro E., Barcia J. A. Suppression of the cardiac electric field artifact from the heart action evoked potential. Med. Biol. Eng.Comput. 2005. V. 43. P. 572–581. URL: https://doi.10.1007/BF02351030
  42. Pigarev I. N. The visceral theory of sleep. Neurosci. Behav. Physiol. 2014. V. 44. P. 421–434. URL: https://doi.org/10.1007/s11055–014–9928-z
  43. Pigarev I. N., Saalmann Y. B., Vidyasagar T. R. A minimally invasive and reversible system for chronic recordings from multiple brain sites in macaque monkeys. J. Neurosci. Methods. 2009. V. 181. P. 151–158. URL: https://doi: 10.1016/j.jneumeth.2009.04.024
  44. Salameh L., Bitzenhofer S., Hanganu-Opatz I., Dutschmann M., Egger V. Blood pressure pulsations modulate central neuronal activity via mechanosensitive ion channels. Science (New York, N.Y.). 2024. V. 383. Р. eadk8511. URL: https://doi: 10.1126/science.adk8511
  45. Seth A. K., Tsakiris M., Being a beast machine: the somatic basis of selfhood. Trends Cognit. Sci. 2018. V. 22. P. 969–981. URL: https://doi: 10.1016/j.tics.2018.08.008
  46. Tallon-Baudry C., Campana F., Park H-D., Babo-Rebelo M. The neural monitoring of visceral inputs, rather than attention, accounts for first-person perspective in conscious vision. Cortex. V. 102. P. 139–149. URL: https://doi: 10.1016/j.cortex.2017.05.019
  47. Tong S., Bezerianos A., Paul J., Zhu Y., Thakor N. Removal of ECG interference from the EEG recordings in small animals using independent component analysis. J. Neurosci. Methods. 2001. V. 108. P. 11–17. URL: https://doi: 10.1016/s0165–0270(01)00366–1. PMID: 11459613
  48. Verberne A. J., Owens M. Cortical modulation of the cardiovascular system. Progress in Neurobiol. 1998. V. 54. P. 149–168. URL: https://doi: 10.1016/s0301–0082(97)00056–7
  49. Whalley K. Olfactory neurons can feel the (heart) beat. Nat. Rev. Neurosci. 2024. V. 25, P. 210. URL: https://doi.org/10.1038/s41583–024–00801–5
  50. Winston J., Rees G. Following your heart. Nat. Neurosci. 2014. V. 17. P. 482–483. URL: https://doi.org/10.1038/nn.3677
  51. Yasui Y., Breder C. D., Saper C. B., Cechetto D. F. Autonomic responses and efferent pathways from the insular cortex in the rat. J. Comp. Neurol. 1991. V. 303. P. 355–374. URL: https://doi: 10.1002/cne.903030303.
  52. Yu X. L., Zhang C., Zhang J. B. Causal interactions between the cerebral cortex and the autonomic nervous system. Sci. China Life Sci. 2014. V. 57. P. 532–538. URL: https://doi: 10.1007/s11427–014–4627–0

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