Consciousness: a neurosurgical perspective.
Concept cells
Consciousness
Medial frontal lobe
Medial temporal lobe
Single-neuron recordings
Volition
Journal
Acta neurochirurgica
ISSN: 0942-0940
Titre abrégé: Acta Neurochir (Wien)
Pays: Austria
ID NLM: 0151000
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
received:
02
12
2022
accepted:
24
07
2023
medline:
23
10
2023
pubmed:
18
8
2023
entrez:
18
8
2023
Statut:
ppublish
Résumé
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.
Identifiants
pubmed: 37594639
doi: 10.1007/s00701-023-05738-9
pii: 10.1007/s00701-023-05738-9
doi:
Types de publication
Journal Article
Review
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
2729-2735Subventions
Organisme : NINDS NIH HHS
ID : U01 NS108930
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS084017
Pays : United States
Organisme : NINDS NIH HHS
ID : U01 NS123128
Pays : United States
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.
Références
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
doi: 10.1006/ccog.1999.0423
pubmed: 10993665
Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322(5903):876–880. https://doi.org/10.1126/science.1149213
doi: 10.1126/science.1149213
pubmed: 18988836
pmcid: 2743249
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
doi: 10.3171/2019.3.JNS183429
pubmed: 31200379
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
doi: 10.1016/j.brs.2019.08.011
pubmed: 31474544
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
doi: 10.1016/j.brs.2020.09.003
pubmed: 32927093
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
doi: 10.1073/pnas.1902276116
pubmed: 31871144
pmcid: 6936686
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
doi: 10.1371/journal.pone.0021612
pubmed: 21760881
pmcid: 3124546
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
doi: 10.1126/scitranslmed.3006294
pubmed: 23946194
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
doi: 10.1038/nature09510
pubmed: 20981100
pmcid: 3010923
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
doi: 10.1016/j.neuron.2022.05.007
pubmed: 35679860
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
doi: 10.1227/01.neu.0000129279.26534.76
pubmed: 15271233
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
doi: 10.1016/s0010-0277(00)00123-2
pubmed: 11164022
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
doi: 10.1073/pnas.95.24.14529
pubmed: 9826734
pmcid: 24407
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
doi: 10.1073/pnas.1332574100
pubmed: 12829797
pmcid: 166261
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
Dennett DC (1993) Consciousness explained. Penguin Books, London
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
doi: 10.1126/science.1169896
pubmed: 19423830
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
doi: 10.1038/s41582-020-00428-x
pubmed: 33318675
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
doi: 10.1212/WNL.0000000000003404
pubmed: 27815400
pmcid: 5177681
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
doi: 10.1073/pnas.1700148114
pubmed: 28743752
pmcid: 5558998
Fried I (2021) Neurons as will and representation. Nat Rev Neurosci 23(2):104–114. https://doi.org/10.1038/s41583-021-00543-8
doi: 10.1038/s41583-021-00543-8
pubmed: 34931068
pmcid: 9359715
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
doi: 10.1523/JNEUROSCI.11-11-03656.1991
pubmed: 1941101
pmcid: 6575551
Fried I, Wilson CL, MacDonald KA, Behnke EJ (1998) Electric current stimulates laughter. Nature 391(6668):650–650
doi: 10.1038/35536
pubmed: 9490408
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
doi: 10.1016/j.neuron.2010.11.045
pubmed: 21315264
pmcid: 3052770
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
doi: 10.1016/j.brs.2021.11.020
pubmed: 34864240
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
doi: 10.1016/j.tins.2018.04.009
pubmed: 29933770
pmcid: 6024487
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
doi: 10.1126/science.1164685
pubmed: 18772395
pmcid: 2650423
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
doi: 10.1038/s41467-018-03749-0
pubmed: 29802308
pmcid: 5970215
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
doi: 10.1093/brain/113.6.1673
pubmed: 2276040
Haggard P (2008) Human volition: towards a neuroscience of will. Nat Rev Neurosci 9(12):934–946. https://doi.org/10.1038/nrn2497
doi: 10.1038/nrn2497
pubmed: 19020512
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
doi: 10.1038/s41593-022-01107-4
pubmed: 35817847
pmcid: 9276533
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
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
doi: 10.1038/78868
pubmed: 10966627
Kreiman G, Koch C, Fried I (2000) Imagery neurons in the human brain. Nature 408:357–361. https://doi.org/10.1038/35042575
doi: 10.1038/35042575
pubmed: 11099042
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
doi: 10.1073/pnas.072194099
pubmed: 12034865
pmcid: 123075
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
doi: 10.1073/pnas.1917251117
pubmed: 32398367
pmcid: 7261054
León F, Zahavi D (2022) Consciousness, philosophy, and neuroscience. Acta Neurochir. https://doi.org/10.1007/s00701-022-05179-w
doi: 10.1007/s00701-022-05179-w
pubmed: 35320396
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
doi: 10.1093/brain/106.3.623
pubmed: 6640273
Lionel N (2018) Minimally conscious state or cortically mediated state? Brain 141(4):949–960. https://doi.org/10.1093/brain/awx324
doi: 10.1093/brain/awx324
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
doi: 10.1093/nc/niab028
pubmed: 34513028
pmcid: 8415036
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
doi: 10.1523/JNEUROSCI.1640-08.2008
pubmed: 18768680
pmcid: 2676868
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
doi: 10.1038/nn.2899
pubmed: 21874014
pmcid: 3505687
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
doi: 10.1016/j.neuron.2015.09.018
pubmed: 26447581
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
doi: 10.1126/science.aax1030
pubmed: 31416934
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
doi: 10.1016/j.tics.2009.11.001
pubmed: 19969501
pmcid: 2806969
Penfield W (1958) Some mechanisms of consciousness discovered during electrical stimulation of the brain. Proc Natl Acad Sci USA 44(2):51
doi: 10.1073/pnas.44.2.51
pubmed: 16590173
pmcid: 335365
Penfield W, Jasper H (1954) Epilepsy and the functional anatomy of the human brain. Little, Brown & Co, Boston
Penfield W, Perot P (1963) The brain’s record of auditory and visual experience: a final summary and discussion. Brain 86(4):595–696
doi: 10.1093/brain/86.4.595
pubmed: 14090522
Penfield W, Roberts L (1959) Speech and brain mechanisms. Princeton University Press, Princeton
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
doi: 10.1162/jocn_a_00799
pubmed: 25761001
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
doi: 10.1007/s10143-021-01566-6
pubmed: 33993354
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
doi: 10.1093/med/9780190208875.001.0001
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
doi: 10.1038/nature03687
pubmed: 15973409
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
doi: 10.1073/pnas.0707043105
pubmed: 18299568
pmcid: 2265174
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
doi: 10.1016/j.neuron.2014.09.006
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
doi: 10.1016/j.cub.2017.08.025
pubmed: 28943091
Rosenthal D (2005) Consciousness and mind. Oxford University Press, Oxford
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
doi: 10.1016/j.cub.2011.08.035
pubmed: 21962712
pmcid: 4574690
Schiff ND (2018) Resolving the role of the paramedian thalamus in forebrain arousal mechanisms. Ann Neurol 84:812–813
doi: 10.1002/ana.25378
pubmed: 30421449
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
doi: 10.1073/pnas.1210467109
pubmed: 22869750
pmcid: 3479453
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
doi: 10.3389/fnhum.2010.00046
pubmed: 20577584
pmcid: 2889679
Sjöberg RL (2022) Brain stimulation and elicited memories. Acta Neurochir. https://doi.org/10.1007/s00701-022-05307-6
doi: 10.1007/s00701-022-05307-6
pubmed: 35804269
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
doi: 10.1038/nn.2112
pubmed: 18408715
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
doi: 10.1038/s41583-023-00692-y
pubmed: 37046077
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
doi: 10.1038/nrn.2016.44
pubmed: 27225071
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
doi: 10.1126/science.aau8956
pubmed: 30819961
pmcid: 6478623
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
doi: 10.1126/science.aba0672
pubmed: 32139543
pmcid: 7211396
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
doi: 10.1523/JNEUROSCI.2101-06.2006
pubmed: 17021178
pmcid: 6674629
Weiskrantz L (1997) Consciousness lost and found: a neuropsychological exploration. Oxford University Press, Oxford
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
doi: 10.1038/s41562-021-01284-5
pubmed: 35190711