Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-23T15:44:36.644Z Has data issue: false hasContentIssue false
  • English
  • Français

The World of Touch – From Evoked Potentials to Conscious Perception

Published online by Cambridge University Press:  05 August 2019

Alan J. McComas
Alan J. McComas*
Affiliation:
Department of Medicine (Division of Neurology), McMaster University, Hamilton
*
McMaster University Health Sciences Centre, Department of Medicine (Division of Neurology), 1200 Main Street West, Hamilton, Ontario, Canada L8N 3Z5
Rights & Permissions [Opens in a new window]

Abstract:

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Microelectrode recordings have enabled several maps of the body surface to be recognized in the mammalian somatosensory cortex. The maps appear to represent increasingly complex levels of analysis of the sensory message. At present the prevailing opinion is that the different components of the ERPs (event related potentials) represent sequential steps in such an analysis, and such an interpretation is supported by the enhancement of the ERPs when attention is paid to a somatic stimulus. However, there are a number of critical observations which are inconsistent with this view and suggest that the ERP enhancement may be an epiphenomenon. An alternative explanation for the ERPs is that they reflect discharges from the non-specific thalamic nuclei, and are essentially similar to the long latency responses which can be recorded from the cortex during sleep or anaesthesia. Lastly, a hypothesis is proposed for the neuronal events in the somatosensory cortex which culminate in a conscious perception. In this “RULER” model, the deep pyramidal neurones read out the sensory information which has been retained in the apical dendrites of more superficial cells, and do so at the end of successive “time-chunks”.

Résumé:

Résumé:

Les enregistrements par microélectrodes ont permis d'établir plusieurs cartes de la surface du corps dans le cortex somesthésique de mammifères. Ces cartes semblent représenter des niveaux de plus en plus complexes d'analyse des messages sensitifs. Actuellement, l'opinion courante est que les différentes composantes des potentiels liés aux événements (PREs) représentent des étapes séquentielles dans cette analyse et cette interprétation est supportée par le rehaussement des PREs quand on considère le stimulus somatique. Cependant, il existe un certain nombre d'observations critiques qui sont incompatibles avec cette interprétation et qui suggèrent que le rehaussement des PREs pourrait être un épiphénomène. Une autre explication des PREs est qu'ils reflètent des décharges de noyaux thalamiques non spécifiques et sont essentiellement semblables aux réponses à longue latence qui peuvent être enregistrées dans le cortex pendant le sommeil ou l'anesthésie. Finalement, nous proposons une hypothèse expliquant les événements neuronaux dans le cortex somesthésique dont le point culminant est la perception consciente. Dans le modèle “RULER”, les neurones pyramidaux profonds lisent l'information sensitive qui a été retenue dans les dendrites apicaux de cellules plus superficielles et le font à la fin de “portions de temps” successives.

Type
Review Article
Information
Canadian Journal of Neurological Sciences , Volume 26 , Issue 1 , February 1999 , pp. 7 - 17
Copyright
Copyright © The Canadian Journal of Neurological 1999

References

1. Dawson, GD. Cerebral responses to electrical stimulation of peripheral nerve in man. J Neurol Neurosurg Psychiatry 1947; 10: 134–140.Google Scholar
2. Dawson, GD. Cerebral responses to nerve stimulation in man. Br Med Bull 1950; 6: 326–329.Google Scholar
3. Dawson, GD. A summation technique for the detection of small evoked potentials. Electroencephalogr Clin Neurophysiol 1954; 6: 65–84.Google Scholar
4. Aminoff, MJ, Eisen, AA. AAEM Minimonograph 19: somatosensory evoked potentials. Muscle Nerve 1998; 21: 277–290.Google Scholar
5. Giblin, DR. Somatosensory evoked potentials in healthy subjects and in patients with lesions of the nervous system. Ann NY Acad Sci 1964; 112: 93–142.Google Scholar
6. Chiappa, KH, Hill, RA. Short-latency somatosensory evoked potentials: interpretation. In: Chiappa, KH, ed. Evoked Potentials in Clinical Medicine, 3rd edn. Philadelphia: Lippincott-Raven, 1997: 341–400.Google Scholar
7. Mauguière, F, Desmedt, JE. Bilateral somatosensory evoked potentials in four patients with longstanding surgical hemispherectomy. Ann Neurol 1989; 26: 724–731.Google Scholar
8. McComas, AJ, Wilson, P Martin-Rodriguez, J, Wallace, C, Hankinson, J. Properties of somatosensory neurones in the human thalamus. J Neurol Neurosurg Psychiatry 1970; 33: 716–717.Google Scholar
9. Lueders, H, Lesser, RP, Hahn, J, Dinner, DS, Klem, G. Cortical somatosensory evoked potentials in response to hand stimulation. J Neurosurg 1983; 58: 885–894.Google Scholar
10. Papakostopoulos, D, Cooper, R, Crow, HJ. Inhibition of cortical evoked potentials and sensation by self-initiated movement in man. Nature 1975; 258: 321–324.Google Scholar
11. Jiang, W, Chapman, CE, Lamarre, Y. Modulation of the cutaneous responsiveness of neurones in the primary somatosensory cortex during conditioned arm movements in the monkey. Exp Brain Res 1961; 84: 342–354.Google Scholar
12. Dawson, GD. The effect of cortical stimulation on transmission through the cuneate nucleus in the anaesthetized rat. J Physiol (Lond) 1958; 142: 2–3P.Google Scholar
13. Halliday, AM. Clinical applications of evoked potentials. In: Matthews, WB, Glaser, GH, eds. Recent Advances in Clinical Neurology. Edinburgh: Churchill Livingstone, 1978: 47–73.Google Scholar
14. Penfield, W, Boldrey, E. Somatic motor and sensory representation in the cerebral cortex of man as studied by electrical stimulation. Brain 1937; 60: 389–448.Google Scholar
15. Adrian, ED. Double representation of the feet in the sensory cortex of the cat. J Physiol (Lond) 1940; 98: 16–18.Google Scholar
16. Woolsey, CN. “Second” somatic receiving areas in the cerebral cortex of cat, dog and monkey. Fed Proc 1943; 2: 55.Google Scholar
17. Nelson, RJ, Sur, M, Kaas, JH. The organization of the second somatosensory area (Sm II) of the grey squirrel. J Comp Neurol 1979; 184: 473–490.Google Scholar
18. Powell, TPS, Mountcastle, VB. Some aspects of the functional organization of the cortex of the postcentral gyrus of the monkey: a correlation of findings obtained in a single unit analysis with cytoarchitecture. Bull Johns Hopkins Hosp 1959; 105: 133–162.Google Scholar
19. Kaas, JH, Nelson, RJ, Sur, M, Lin, C-S, Merzenich, MM. Multiple representations of the body within the primary somatosensory cortex of primates. Science 1979; 204: 521–523.Google Scholar
20. Kaas, A. What, if anything, is SI? Organization of first somatosensory area of cortex. Physiol Rev 1983; 63: 206–231.Google Scholar
21. Sutton, S, Braren, M, Zubin, J, John, ER. Evoked-potential correlates of stimulus uncertainty. Science 1965; 150: 1187–1188.Google Scholar
22. Desmedt, JE, Tomberg, C. Mapping early somatosensory evoked potentials in selective attention: critical evaluation of control conditions used for titrating by; difference the cognitive P30, P40, P100 and N140 . Electroencephalogr Clin Neurophysiol 1989; 74: 321–346.Google Scholar
23. Desmedt, JE, Tomberg, C. The search for “neutral” conditions for recording control event-related potentials in order to assess cognitive components to both irrelevant and relevant stimuli: evidence for short-latency cognitive somatosensory effects. Electroencephalogr Clin Neurophysiol 1991; (Suppl 42): 210–221.Google Scholar
24. Tomberg, C, Noël, P Ozaki, I, Desmedt, JE. Inadequacy of the average reference for the topographic mapping of focal enhancements of brain potentials. Electroencephalogr Clin Neurophysiol 1990; 77: 259–265.Google Scholar
25. Felleman, DJ, Van Essen, DC. Distributed hierarchical processing in the primate cerebral cortex. Cerebral Cortex 1991; 1: 1–47.Google Scholar
26. Friedman, DP, Murray, EA, O’Neil, B, Mishkin, M. Cortical connections of the somatosensory fields of the lateral sulcus of Macaques: evidence of a corticolimbic pathway for touch. J Comp Neurol 1986; 252: 323–347.Google Scholar
27. Hillyard, SA. Electrophysiology of human selective attention. Trends Neurosci 1985; 8: 400–405.Google Scholar
28. Tomberg, C, Desmedt, JE. Non-averaged human brain potentials in somatic attention: the short-latency cognition-related P40 component. J Physiol (Lond) 1996; 496: 559–574.Google Scholar
29. Creutzfeldt, OD. Cortex Cerebri. Performance, Structure and Functional Organization of the Cortex. Oxford: Oxford University Press, 1994: 199–205.Google Scholar
30. Desmedt, JE, Debecker, J. Waveforms and neural mechanism of the decision P300 elicited without prestimulus CNV or readiness potential. Electroencephalogr Clin Neurophysiol 1979; 47: 648–670.Google Scholar
31. Libet, B, Alberts, WW, Wright, EW Jr, et al. Production of threshold levels of conscious sensation by electrical stimulation of human somatosensory cortex. J Neurophysiol 1964; 27: 546–578.Google Scholar
32. Gardner, EP. Somatosensory cortical mechanisms of feature detection in tactile and kinesthetic discrimination. Can J Physiol Pharmacol 1988; 66: 439–454.Google Scholar
33. Hollerbach, S, Tougas, G, Frieling, T, et al. Cerebral evoked responses to gastrointestinal stimulation in human. Crit Rev Biomed Engin 1997; 25: 203–242.Google Scholar
34. Li, C-L, Cullen, C, Jasper, HH. Laminar microelectrode studies of specific somatosensory cortical potentials. J Neurophysiol 1956; 19: 111–130.Google Scholar
35. Loomis, AL, Harvey, EN, Hobart, GA. Disturbance-patterns in sleep. J Neurophysiol 1938; 1: 413–430.Google Scholar
36. Halliday, AM, Mason, AA. The effect of hypnotic anaesthesia on cortical responses. J Neurol Neurosurg Psychiatry 1964; 27: 300–312.Google Scholar
37. Morison, RS, Dempsey, EW. A study of thalamocortical relations. J Neurophysiol 1942; 135: 280–292.Google Scholar
38. Jasper, HH, Ajmone-Marsan, C. Thalamocortical integrating mechanisms. Res Publ Assoc Nervous Mental Disorders 1952; 30: 493–512.Google Scholar
39. Steriade, M. The excitatory-inhibitory response sequence in thalamic and neocortical cells: state-related changes and regulatory systems. In: Edelman, GM, Gall, WE, Cowan, WM, eds. Dynamic Aspects of Neocortical Function. New York: Wiley, 1984: 107–157.Google Scholar
40. Ropert, N, Steriade, M. Input-output organization of midbrain reticular area. J Neurophysiol 1981; 46: 17–31.Google Scholar
41. Hobson, JA, Steriade, M. Neuronal basis of behavioural state control. In: Mountcastle, VB, Bloom, FE, eds. Handbook of Physiology. Bethesda, MD: American Physiological Society 1984: 701–823.Google Scholar
42. Starzl, TE, Taylor, CW, Magoun, HW. Collateral afferent excitation of reticular formation of brain stem. J Neurophysiol 1951; 46: 17–31.Google Scholar
43. Albe-Fessard, D, Besson, JM. Convergent thalamic and cortical projections – the non-specific system. In: Iggo, A, ed. Handbook of Sensory Physiology, vol 2: Somatosensory System. Berlin: Springer-Verlag 1973: 489–560.Google Scholar
44. Adrian, ED. Afferent discharges to the cerebral cortex from peripheral sense organs. J Physiol (Lond) 1941; 100: 159–191.Google Scholar
45. McComas, AJ. Containing the contents. In: Jasper, HH, Descarries, L, Castellucci, VE, Rossignol, S, eds. Consciousness – at the Frontiers of Neuroscience. New York: Lippincott-Raven. Adv Neurol, 1998; 77: 135–148.Google Scholar
46. Merzenich, MM, Schreiner, C, Jenkins, W, Wane, X. Neural mechanisms underlying temporal integration, segmentation, and input sequence representation: some implications for the origin of learning disabilities. Ann NY Acad Sci 1993; 682: 1–22.Google Scholar
47. MacIntyre, NJ, McComas, AJ. Non-conscious choice in cutaneous backward masking. NeuroReport 1996; 7: 1513–1516.Google Scholar
48. Hirsch, IJ, Sherrick, CE. Perceived order in different sense modalities. J Exp Psychol 1961; 62: 423–432.Google Scholar
49. Purves, D, Paydarfar, JA, Andrews, TJ. The wagon wheel in movies and reality. Proc Natl Acad Sci USA 1996; 93: 3693–3697.Google Scholar
50. Hellweg, F-C, Schultz, W, Creutzfeldt, OD. Extracellular and intracellular recordings from cat’s cortical whisker projection area: thalamocortical response transformation. J Neurophysiol 1977; 40: 463–479.Google Scholar
51. Amassian, VE. Evoked single cortical unit activity in the somatic sensory areas. Electroencephalogr Clin Neurophysiol 1953; 5: 415–438.Google Scholar
52. Kulics, AT, Cauller, LJ. Cerebral cortical somatosensory evokedresponses, multiple unit activity and current source-densities: their interrelationships and significance to somatic sensation as revealed by stimulation of the awake monkey’s hand. Exp Brain Res 1986; 62: 46–60.Google Scholar
53. Lorente de Nó, R. Cerebral cortex: Architecture, intracortical connections, motor projections. In: Fulton, JF. Physiology of the Nervous System, 3rd edn. New York: Oxford University Press, 1949: 288–320.Google Scholar
54. Peters, A, Sethares, C. Myelinated axons and the pyramidal cell modules in monkey primary visual cortex. J Comp Neurol 1996; 365: 232–255.Google Scholar
55. Cobb, SR, Buhl, EH, Halasy, K, Paulsen, O, Somogyi, P. Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons. Nature 1995; 378: 75–78.Google Scholar
56. Walter, WG, Cooper, R, Alridge, VJ, McCallum, WC, Winter, AL. Contingent negative variation: an electric sign of sensorimotor association and expectancy in the human brain. Nature 1964; 203: 380–384.Google Scholar
57 Näätänen, R. Processing negativity: an evoked-potential reflection of selective attention. Psychol Bull 1982; 92: 605–640.Google Scholar
58. Goldring, S, O’Leary, JL, King, RB. Singly and repetitively evoked potential in human cerebral cortex with D.C. changes. Electroencephalogr Clin Neurophysiol 1958; 10: 233–240.Google Scholar