Skip to main content

Advertisement

SpringerLink
Log in

Consciousness: a neurosurgical perspective

  • Mini-review (by Invitation)
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Neurosurgeons are in a unique position to shed light on the neural basis for consciousness, not only by their clinical care of patients with compromised states of consciousness, but also by employing neurostimulation and neuronal recordings through intracranial electrodes in awake surgical patients, as well as during stages of sleep and anethesia. In this review, we discuss several aspects of consciousness, i.e., perception, memory, and willed actions, studied by electrical stimulation and single neuron recordings in the human brain. We demonstrate how specific neuronal activity underlie the emergence of concepts, memories, and intentions in human consciousness. We discuss the representation of specific conscious content by temporal lobe neurons and present the discovery of “concept cells” and the encoding and retrieval of memories by neurons in the medial temporal lobe. We review prefrontal and parietal neuronal activation that precedes conscious intentions to act. Taken together with other studies in the field, these findings suggest that specific conscious experience may arise from stochastic fluctuations of neuronal activity, reaching a dynamic threshold. Advances in brain recording and stimulation technology coupled with the rapid rise in artificial intelligence are likely to increase the amount and analysis capabilities of data obtained from the human brain, thereby improving the decoding of conscious and preconscious states and open new horizons for modulation of human cognitive functions such as memory and volition.

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

Similar content being viewed by others

References

  1. Alkire MT, Haier RJ, Fallon JH (2000) Toward a unified theory of narcosis: brain imaging evidence for a thalamocortical switch as the neurophysiologic basis of anesthetic-induced unconsciousness. Conscious Cogn 9:370–386

    Article  CAS  PubMed  Google Scholar 

  2. Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322(5903):876–880. https://doi.org/10.1126/science.1149213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Andelman-Gur MM, Gazit T, Andelman F, Kipervasser S, Kramer U et al (2019) Spatial distribution and hemispheric asymmetry of electrically evoked experiential phenomena in the human brain. J Neurosurg 133(1):54–62. https://doi.org/10.3171/2019.3.JNS183429

    Article  PubMed  Google Scholar 

  4. Andelman-Gur MM, Gazit T, Fahoum F, Andelman F, Fried I (2019) Negative and positive volitional responses induced by stimulating the superior frontal gyrus: a case study. Brain Stimul 12(6):1614–1616. https://doi.org/10.1016/j.brs.2019.08.011

    Article  PubMed  Google Scholar 

  5. Andelman-Gur MM, Gazit T, Strauss I, Fried I, Fahoum F (2020) Stimulating the inferior fronto-occipital fasciculus elicits complex visual hallucinations. Brain Stimul 13(6):1577–1579. https://doi.org/10.1016/j.brs.2020.09.003

    Article  PubMed  Google Scholar 

  6. Andersen RA, Aflalo T, Kellis S (2019) From thought to action: the brain–machine interface in posterior parietal cortex. Proc Natl Acad Sci U S A 116(52):26274–26279. https://doi.org/10.1073/pnas.1902276116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Bode S, He AH, Soon CS, Trampel R, Turner R et al (2011) Tracking the unconscious generation of free decisions using uitra-high field fMRI. PLoS One 6(6):e21612. https://doi.org/10.1371/journal.pone.0021612

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Casali AG, Gosseries O, Rosanova M, Boly M, Sarasso S et al (2013) A theoretically based index of consciousness independent of sensory processing and behavior. Sci Transl Med 5(198):198ra105. https://doi.org/10.1126/scitranslmed.3006294

    Article  PubMed  Google Scholar 

  9. Cerf M, Thiruvengadam N, Mormann F, Kraskov A, Quiroga RQ et al (2010) On-line, voluntary control of human temporal lobe neurons. Nature 467(7319):1104–1108. https://doi.org/10.1038/nature09510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Chung JE, Sellers KK, Leonard MK, Gwilliams L, Xu D et al (2022) High-density single-unit human cortical recordings using the Neuropixels probe. Neuron 110(15):2409-2421.e3. https://doi.org/10.1016/j.neuron.2022.05.007

    Article  CAS  PubMed  Google Scholar 

  11. Crick F, Koch C, Kreiman G, Fried I (2004) Consciousness and neurosurgery. Neurosurgery 55(2):273–282. https://doi.org/10.1227/01.neu.0000129279.26534.76

    Article  PubMed  Google Scholar 

  12. Dehaene S, Naccache L (2001) Towards a cognitive neuroscience of consciousness: basic evidence and a workspace framework. Cognition 79(1–2):1–37. https://doi.org/10.1016/s0010-0277(00)00123-2

    Article  CAS  PubMed  Google Scholar 

  13. Dehaene S, Kerszberg M, Changeux JP (1998) A neuronal model of a global workspace in effortful cognitive tasks. Proc Natl Acad Sci USA 95(24):14529–14534. https://doi.org/10.1073/pnas.95.24.14529

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Dehaene S, Sergent C, Changeux JP (2003) A neuronal network model linking subjective reports and objective physiological data during conscious perception. Proc Natl Acad Sci USA 100(14):8520–8525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Dehaene S, Changeux JP, Naccache L (2011) The Global Neuronal Workspace Model of Conscious Access: from neuronal architectures to clinical applications. In: Dehaene S, Christen Y (eds) Characterizing Consciousness: From Cognition to the Clinic? Research and Perspectives in Neurosciences. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-18015-6_4

  16. Dennett DC (1993) Consciousness explained. Penguin Books, London

  17. Desmurget M, Reilly KT, Richard N, Szathmari A, Mottolese C et al (2009) Movement intention after parietal cortex stimulation in humans. Science 324(5928):811–813. https://doi.org/10.1126/science.1169896

    Article  CAS  PubMed  Google Scholar 

  18. Edlow BL, Claassen J, Schiff ND, Greer DM (2021) Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nat Rev Neurol 17:135–156. https://doi.org/10.1038/s41582-020-00428-x

    Article  PubMed  Google Scholar 

  19. Fischer DB, Boes AD, Demertzi A, Evrard HC, Laureys S (2016) A human brain network derived from coma-causing brainstem lesions. Neurology 87:2427–2434

    Article  PubMed  PubMed Central  Google Scholar 

  20. Flores FJ, Hartnack KE, Fath AB, Kim SE, Wilson MA et al (2017) Thalamocortical synchronization during induction and emergence from propofol-induced unconsciousness. Proc Natl Acad Sci USA 114:E6660–E6668

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Fried I (2021) Neurons as will and representation. Nat Rev Neurosci 23(2):104–114. https://doi.org/10.1038/s41583-021-00543-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Fried I, Katz A, McCarthy G, Sass KJ, Williamson P et al (1991) Functional organization of human supplementary motor cortex studied by electrical stimulation. J Neurosci 11(11):3656–3666. https://doi.org/10.1523/JNEUROSCI.11-11-03656.1991

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Fried I, Wilson CL, MacDonald KA, Behnke EJ (1998) Electric current stimulates laughter. Nature 391(6668):650–650

    Article  CAS  PubMed  Google Scholar 

  24. Fried I, Mukamel R, Kreiman G (2011) Internally generated preactivation of single neurons in human medial frontal cortex predicts volition. Neuron 69(3):548–562. https://doi.org/10.1016/j.neuron.2010.11.045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Fried I, Fahoum F, Frew A, Andelman F, Andelman-Gur MM et al (2022) Laser ablation of human guilt. Brain Stimul 15(1):164–166. https://doi.org/10.1016/j.brs.2021.11.020

    Article  PubMed  Google Scholar 

  26. Frith CD, Haggard P (2018) Volition and the brainrevisiting a classic experimental study. Trends Neurosci 41(7):405–407. https://doi.org/10.1016/j.tins.2018.04.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322(5898):96–101. https://doi.org/10.1126/science.1164685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Gelbard-Sagiv H, Mudrik L, Hill MR, Koch C, Fried I (2018) Human single neuron activity precedes emergence of conscious perception. Nat Commun 9:2057. https://doi.org/10.1038/s41467-018-03749-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Gloor P (1990) Experiential phenomena of temporal lobe epilepsy. Facts and hypotheses. Brain 113(Pt 6):1673–1694. https://doi.org/10.1093/brain/113.6.1673

    Article  PubMed  Google Scholar 

  30. Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9(12):934–946. https://doi.org/10.1038/nrn2497

    Article  CAS  PubMed  Google Scholar 

  31. Hayat H, Marmelshtein A, Krom AJ, Sela Y, Tankus A et al (2022) Reduced neural feedback signaling despite robust neuron and gamma auditory responses during human sleep. Nat Neurosci 25:935–943. https://doi.org/10.1038/s41593-022-01107-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Jackson JH (1931) Lectures on the diagnosis of epilepsy. In: Taylor J (ed) Selected Writings of John Hughlings Jackson. Holder and Stoughton, London, pp 276–307

    Google Scholar 

  33. Kreiman G, Koch C, Fried I (2000) Category-specific visual responses of single neurons in the human medial temporal lobe. Nat Neurosci 3(9):946–953. https://doi.org/10.1038/78868

    Article  CAS  PubMed  Google Scholar 

  34. Kreiman G, Koch C, Fried I (2000) Imagery neurons in the human brain. Nature 408:357–361. https://doi.org/10.1038/35042575

    Article  CAS  PubMed  Google Scholar 

  35. Kreiman G, Fried I, Koch C (2002) Single-neuron correlates of subjective vision in the human medial temporal lobe. Proc Natl Acad Sci USA 99(12):8378–8383. https://doi.org/10.1073/pnas.072194099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Krom AJ, Marmelshtein A, Gelbard-Sagiv H, Tankus A, Hayat H et al (2020) Anesthesia-induced loss of consciousness disrupts auditory responses beyond primary cortex. Proc Natl Acad Sci USA 117(21):11770–11780. https://doi.org/10.1073/pnas.1917251117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. León F, Zahavi D (2022) Consciousness, philosophy, and neuroscience. Acta Neurochir. https://doi.org/10.1007/s00701-022-05179-w

    Article  PubMed  Google Scholar 

  38. Libet B, Gleason CA, Wright EW, Pearl DK (1983) Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. Brain 106(Pt 3):623–642. https://doi.org/10.1093/brain/106.3.623

    Article  PubMed  Google Scholar 

  39. Lionel N (2018) Minimally conscious state or cortically mediated state? Brain 141(4):949–960. https://doi.org/10.1093/brain/awx324

    Article  Google Scholar 

  40. Malach R (2021) Local neuronal relational structures underlying the contents of human conscious experience. Neurosci Conscious 2021(2):niab028. https://doi.org/10.1093/nc/niab028

    Article  PubMed  PubMed Central  Google Scholar 

  41. Mormann F, Kornblith S, Quiroga RQ, Kraskov A, Cerf M et al (2008) Latency and selectivity of single neurons indicate hierarchical processing in the human medial temporal lobe. J Neurosci 28(36):8865–8872. https://doi.org/10.1523/JNEUROSCI.1640-08.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mormann F, Dubois J, Kornblith S, Milosavljevic M, Cerf M et al (2011) A category-specific response to animals in the right human amygdala. Nat Neurosci 14(10):1247–1249. https://doi.org/10.1038/nn.2899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Moutard C, Dehaene S, Malach R (2015) Spontaneous fluctuations and non-linear ignitions: two dynamic faces of cortical recurrent loops. Neuron 88(1):194–206. https://doi.org/10.1016/j.neuron.2015.09.018

    Article  CAS  PubMed  Google Scholar 

  44. Norman Y, Yeagle EM, Khuvis S, Harel M, Mehta AD et al (2019) Hippocampal sharp-wave ripples linked to visual episodic recollection in humans. Science 365(6454):eaax1030. https://doi.org/10.1126/science.aax1030

    Article  CAS  PubMed  Google Scholar 

  45. Passingham RE, Bengtsson SL, Lau HC (2010) Medial frontal cortex: from self-generated action to reflection on one’s own performance. Trends Cogn Sci 14(1):16–21. https://doi.org/10.1016/j.tics.2009.11.001

    Article  PubMed  PubMed Central  Google Scholar 

  46. Penfield W (1958) Some mechanisms of consciousness discovered during electrical stimulation of the brain. Proc Natl Acad Sci USA 44(2):51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little, Brown & Co, Boston

  48. Penfield W, Perot P (1963) The brain’s record of auditory and visual experience: a final summary and discussion. Brain 86(4):595–696

    Article  CAS  PubMed  Google Scholar 

  49. Penfield W, Roberts L (1959) Speech and brain mechanisms. Princeton University Press, Princeton

    Google Scholar 

  50. Perez O, Mukamel R, Tankus A, Rosenblatt JD, Yeshurun Y et al (2015) Preconscious prediction of a driver’s decision using intracranial recordings. J Cogn Neurosci 27(8):1492–1502. https://doi.org/10.1162/jocn_a_00799

    Article  PubMed  Google Scholar 

  51. Pinson H, Van Lerbeirghe J, Vanhauwaert D, Van Damme O, Hallaert G et al (2022) The supplementary motor area syndrome: a neurosurgical review. Neurosurg Rev 45:81–90. https://doi.org/10.1007/s10143-021-01566-6

    Article  PubMed  Google Scholar 

  52. Posner JB, Saper CB, Schiff ND, Claassen J (2019) Plum and Posner’s Diagnosis and Treatment of Stupor and Coma, 5th edn. Oxford Academic Press, New York

    Book  Google Scholar 

  53. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 435(7045):1102–1107. https://doi.org/10.1038/nature03687

    Article  CAS  PubMed  Google Scholar 

  54. Quiroga RQ, Mukamel R, Isham EA, Malach R, Fried I (2008) Human single-neuron responses at the threshold of conscious recognition. Proc Natl Acad Sci U S A 105(9):3599–3604. https://doi.org/10.1073/pnas.0707043105

    Article  PubMed  PubMed Central  Google Scholar 

  55. Quiroga RQ, Kraskov A, Mormann F, Fried I, Koch C (2014) Single-cell responses to face adaptation in the human medial temporal lobe. Neuron 84(2):363–369. https://doi.org/10.1016/j.neuron.2014.09.006

    Article  CAS  Google Scholar 

  56. Reber TP, Faber J, Niediek J, Boström J, Elger CE et al (2017) Single-neuron correlates of conscious perception in the human medial temporal lobe. Curr Biol 27(19):2991-2998.e2. https://doi.org/10.1016/j.cub.2017.08.025

    Article  CAS  PubMed  Google Scholar 

  57. Rosenthal D (2005) Consciousness and mind. Oxford University Press, Oxford

    Google Scholar 

  58. Rutishauser U, Tudusciuc O, Neumann D, Mamelak AN, Heller AC et al (2011) Single-unit responses selective for whole faces in the human amygdala. Curr Biol 21(19):1654–1660. https://doi.org/10.1016/j.cub.2011.08.035

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Schiff ND (2018) Resolving the role of the paramedian thalamus in forebrain arousal mechanisms. Ann Neurol 84:812–813

    Article  PubMed  Google Scholar 

  60. Schurger A, Sitt JD, Dehaene S (2012) An accumulator model for spontaneous neural activity prior to self-initiated movement. Proc Natl Acad Sci USA 109(42):E2904–E2913. https://doi.org/10.1073/pnas.1210467109

    Article  PubMed  PubMed Central  Google Scholar 

  61. Selimbeyoglu A, Parvizi J (2010) Electrical stimulation of the human brain: perceptual and behavioral phenomena reported in the old and new literature. Front Hum Neurosci 4:46. https://doi.org/10.3389/fnhum.2010.00046

    Article  PubMed  PubMed Central  Google Scholar 

  62. Sjöberg RL (2022) Brain stimulation and elicited memories. Acta Neurochir. https://doi.org/10.1007/s00701-022-05307-6

    Article  PubMed  Google Scholar 

  63. Soon CS, Brass M, Heinze HJ, Haynes JD (2008) Unconscious determinants of free decisions in the human brain. Nat Neurosci 11(5):543–545. https://doi.org/10.1038/nn.2112

    Article  CAS  PubMed  Google Scholar 

  64. Stangl M, Maoz SL, Suthana N (2023) Mobile cognition: imaging the human brain in the ‘real world.’ Nat Rev Neurosci. https://doi.org/10.1038/s41583-023-00692-y

    Article  PubMed  Google Scholar 

  65. Tononi G, Boly M, Massimini M, Koch C (2016) Integrated information theory: from consciousness to its physical substrate. Nat Rev Neurosci 17:450–461. https://doi.org/10.1038/nrn.2016.44

    Article  CAS  PubMed  Google Scholar 

  66. Vaz AP, Inati SK, Brunel N, Zaghloul KA (2019) Coupled ripple oscillations between the medial temporal lobe and neocortex retrieve human memory. Science 363(6430):975–978. https://doi.org/10.1126/science.aau8956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Vaz AP, Wittig JH Jr, Inati SK, Zaghloul KA (2020) Replay of cortical spiking sequences during human memory retrieval. Science 367(6482):1131–1134. https://doi.org/10.1126/science.aba0672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Waydo S, Kraskov A, QuianQuiroga R, Fried I, Koch C (2006) Sparse representation in the human medial temporal lobe. J Neurosci 26(40):10232–10234. https://doi.org/10.1523/JNEUROSCI.2101-06.2006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Weiskrantz L (1997) Consciousness lost and found: a neuropsychological exploration. Oxford University Press, Oxford

  70. Yaron I, Melloni L, Pitts M, Mudrik L (2022) The ConTraSt database for analysing and comparing empirical studies of consciousness theories. Nat Hum Behav 6(4):593–604. https://doi.org/10.1038/s41562-021-01284-5

    Article  PubMed  Google Scholar 

Download references

Funding

This work was supported by the National Institute of Health, National Institute of Neurological Disorders and Stroke (NIH NINDS: grants U01NS108930, 1R01NS084017, and U01NS123128 to I.F.), the National Science Foundation (NSF: grant 1756473 to I.F.), and the Azrieli Foundation (Doctoral fellowship to M.A.G.).

Author information

Authors and Affiliations

  1. Department of Brain Sciences, Weizmann Institute of Science, Rehovot, Israel

    Michal M. Andelman-Gur

  2. Department of Neurosurgery, David Geffen School of Medicine and Semel Institute for Neuroscience and Human Behavior, University of California, 300 Stein Plaza, Ste. 562, Los Angeles, CA, USA

    Itzhak Fried

  3. Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel

    Itzhak Fried

Authors
  1. Michal M. Andelman-Gur
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Itzhak Fried
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Itzhak Fried.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Comments

One of the most mind-boggling prospects raised in the mini-review by Andelman-Gur and Fried is that neurosurgeons and neuroscientists may soon be able to use advanced registration and interpretation of neuronal activity to read other people's subjective thoughts, feelings and experiences, even before they occur. Such a technological leap will mean that we have come close to a solution of what philosophers refer to as "the hard problem of consciousness", that is, a technological understanding of the way in which neuronal activity translates to subjective conscious experience.

Honest and informed individuals may disagree about whether the case is overstated and the hard problem is really about to be solved. There are also different but legitimate opinions on some of the views on volition, memory and the mind-brain relationship that the authors build on to make their conjectures. Still, neurosurgeons remain some of the most relevant players in the front line of these discussions and endeavors, that touch upon some of the most central issues of what it means to be human. This mini-review presents an interesting contribution to this literature.

Rickard L Sjoberg

Umea, Sweden

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Andelman-Gur, M.M., Fried, I. Consciousness: a neurosurgical perspective. Acta Neurochir 165, 2729–2735 (2023). https://doi.org/10.1007/s00701-023-05738-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-023-05738-9

Keywords

Search

Navigation