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Experimental Brain Research

, Volume 237, Issue 5, pp 1155–1167 | Cite as

Electrocorticographic changes in field potentials following natural somatosensory percepts in humans

  • Daniel R. KramerEmail author
  • Michael F. Barbaro
  • Morgan Lee
  • Terrance Peng
  • George Nune
  • Charles Y. Liu
  • Spencer Kellis
  • Brian Lee
Research Article

Abstract

Objective

Restoration of somatosensory deficits in humans requires a clear understanding of the neural representations of percepts. To characterize the cortical response to naturalistic somatosensation, we examined field potentials in the primary somatosensory cortex of humans.

Methods

Four patients with intractable epilepsy were implanted with subdural electrocorticography (ECoG) electrodes over the hand area of S1. Three types of stimuli were applied, soft-repetitive touch, light touch, and deep touch. Power in the alpha (8–15 Hz), beta (15–30 Hz), low-gamma (30–50 Hz), and high-gamma (50–125 Hz) frequency bands were evaluated for significance.

Results

Seventy-seven percent of electrodes over the hand area of somatosensory cortex exhibited changes in these bands. High-gamma band power increased for all stimuli, with concurrent alpha and beta band power decreases. Earlier activity was seen in these bands in deep touch and light touch compared to soft touch.

Conclusions

These findings are consistent with prior literature and suggest a widespread response to focal touch, and a different encoding of deeper pressure touch than soft touch.

Keywords

Somatosensory Brain Computer Interface (BCI) Brain Machine Interface (BMI) Electrocorticography Cortical Stimulation 

Notes

Funding

We wish to acknowledge the generous support of Cal-BRAIN: A Neurotechnology Program for California, National Center for Advancing Translational Science (NCATS) of the U.S. National Institutes of Health (KL2TR001854), National Institutes of Health (R25 NS099008-01), The Neurosurgery Research and Education Foundation (NREF), the Tianqiao and Chrissy Chen Brain-machine Interface Center at Caltech, the Boswell Foundation and the Della Martin Foundation, and the University of Southern California Neurorestoration Center. None of the listed sources of funding had a role in study collection, analysis, interpretation of data, or writing of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest involved with this or related work.

Ethical approval

All research herein complies with institutional and international guidelines on research involving human participants, and was conducted after approval by the institutional review board (study approval HS-13-00528). Informed consent was obtained from all individual participants included in the study. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Supplementary material

221_2019_5495_MOESM1_ESM.pdf (496 kb)
Supplementary material 1 (PDF 496 KB)

References

  1. Agnew WF, McCreery DB (1987) Considerations for safety in the use of extracranial stimulation for motor evoked potentials. Neurosurgery 20:143–147 (Epub 1987/01/01) CrossRefGoogle Scholar
  2. Alvarez M, Zainos A, Romo R (2015) Decoding stimulus features in primate somatosensory cortex during perceptual categorization. Proc Natl Acad Sci USA 112:4773–4778 (Epub 2015/04/01) CrossRefGoogle Scholar
  3. Armenta Salas M, Bashford L, Kellis S, Jafari M, Jo H, Kramer D, Shanfield K, Pejsa K, Lee B, Liu CY et al (2018) Proprioceptive and cutaneous sensations in humans elicited by intracortical microstimulation. Elife 7 (Epub 2018/04/11) Google Scholar
  4. Bauer M, Oostenveld R, Peeters M, Fries P (2006) Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci 26:490–501. (Epub 2006/01/13) CrossRefGoogle Scholar
  5. Bauer M, Stenner MP, Friston KJ, Dolan RJ (2014) Attentional modulation of alpha/beta and gamma oscillations reflect functionally distinct processes. J Neurosci 34:16117–16125 (Epub 2014/11/28) CrossRefGoogle Scholar
  6. Bensmaia SJ (2008) Tactile intensity and population codes. Behav Brain Res 190:165–173 (Epub 2008/04/19) CrossRefGoogle Scholar
  7. Birznieks I, Vickery RM (2017) Spike timing matters in novel neuronal code involved in vibrotactile frequency perception. Curr Biol 27:1485–1490.e1482 (Epub 2017/05/10) CrossRefGoogle Scholar
  8. Brinkman L, Stolk A, Dijkerman HC, de Lange FP, Toni I (2014) Distinct roles for alpha- and beta-band oscillations during mental simulation of goal-directed actions. J Neurosci 34:14783–14792 (Epub 2014/10/31) CrossRefGoogle Scholar
  9. Burton H, Sinclair RJ (2000) Attending to and remembering tactile stimuli: a review of brain imaging data and single-neuron responses. J Clin Neurophysiol 17:575–591 (Epub 2001/01/11) CrossRefGoogle Scholar
  10. Crone NE, Miglioretti DL, Gordon B, Lesser RP (1998) Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. Brain 121(Pt 12):2301–2315 (Epub 1999/01/05) CrossRefGoogle Scholar
  11. Crone NE, Sinai A, Korzeniewska A (2006) High-frequency gamma oscillations and human brain mapping with electrocorticography. Prog Brain Res 159:275–295 (Epub 2006/10/31) CrossRefGoogle Scholar
  12. Debener S, Herrmann CS, Kranczioch C, Gembris D, Engel AK (2003) Top-down attentional processing enhances auditory evoked gamma band activity. Neuroreport 14:683–686 (Epub 2003/04/15) CrossRefGoogle Scholar
  13. Engel AK, Fries P, Singer W (2001) Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2:704–716 (Epub 2001/10/05) CrossRefGoogle Scholar
  14. Flesher SN, Collinger JL, Foldes ST, Weiss JM, Downey JE, Tyler-Kabara EC, Bensmaia SJ, Schwartz AB, Boninger ML, Gaunt RA (2016) Intracortical microstimulation of human somatosensory cortex. Sci Transl Med 19(8):361ra141 (Epub 2016/11/01) CrossRefGoogle Scholar
  15. Fries P (2015) Rhythms for cognition: communication through coherence. Neuron 88:220–235 (Epub 2015/10/09) CrossRefGoogle Scholar
  16. Fries P, Reynolds JH, Rorie AE, Desimone R (2001) Modulation of oscillatory neuronal synchronization by selective visual attention. Science 291:1560–1563 (Epub 2001/02/27) CrossRefGoogle Scholar
  17. Gruber T, Muller MM, Keil A, Elbert T (1999) Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin Neurophysiol 110:2074–2085 (Epub 2000/01/01) CrossRefGoogle Scholar
  18. Haegens S, Handel BF, Jensen O (2011) Top-down controlled alpha band activity in somatosensory areas determines behavioral performance in a discrimination task. J Neurosci 31:5197–5204 (Epub 2011/04/08) CrossRefGoogle Scholar
  19. Haegens S, Luther L, Jensen O (2012) Somatosensory anticipatory alpha activity increases to suppress distracting input. J Cogn Neurosci 24:677–685 (Epub 2011/11/10) CrossRefGoogle Scholar
  20. Handel BF, Haarmeier T, Jensen O (2011) Alpha oscillations correlate with the successful inhibition of unattended stimuli. J Cogn Neurosci 23:2494–2502 (Epub 2010/08/05) CrossRefGoogle Scholar
  21. Hauck M, Lorenz J, Engel AK (2007) Attention to painful stimulation enhances gamma-band activity and synchronization in human sensorimotor cortex. J Neurosci 27:9270–9277 (Epub 2007/08/31) CrossRefGoogle Scholar
  22. Hsiao SS, Lane J, Fitzgerald P (2002) Representation of orientation in the somatosensory system. Behav Brain Res 135:93–103. http://chronux.org/ (Epub 2002/10/03)
  23. Khanna P, Carmena JM (2017) Beta band oscillations in motor cortex reflect neural population signals that delay movement onset. Elife (Epub 2017/05/04) Google Scholar
  24. Krebber M, Harwood J, Spitzer B, Keil J, Senkowski D (2015) Visuotactile motion congruence enhances gamma-band activity in visual and somatosensory cortices. Neuroimage 117:160–169 (Epub 2015/06/01) CrossRefGoogle Scholar
  25. Lee B, Kramer D, Armenta Salas M, Kellis S, Brown D, Dobreva T, Klaes C, Heck C, Liu C, Andersen RA (2018) Engineering artificial somatosensation through cortical stimulation in humans. Front Syst Neurosci 12:24CrossRefGoogle Scholar
  26. Liu CC, Chien JH, Chang YW, Kim JH, Anderson WS, Lenz FA (2015) Functional role of induced gamma oscillatory responses in processing noxious and innocuous sensory events in humans. Neuroscience 310:389–400 (Epub 2015/09/27) CrossRefGoogle Scholar
  27. Luna R, Hernandez A, Brody CD, Romo R (2005) Neural codes for perceptual discrimination in primary somatosensory cortex. Nat Neurosci 8:1210–1219 (Epub 2005/08/02) CrossRefGoogle Scholar
  28. Macefield G, Gandevia SC, Burke D (1990) Perceptual responses to microstimulation of single afferents innervating joints, muscles and skin of the human hand. J Physiol 429:113–129 (Epub 1990/10/01) CrossRefGoogle Scholar
  29. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG- and MEG-data. J Neurosci Methods 164:177–190. (Epub 2007/05/23) CrossRefGoogle Scholar
  30. Menon V, Freeman WJ, Cutillo BA, Desmond JE, Ward MF, Bressler SL, Laxer KD, Barbaro N, Gevins AS (1996) Spatio-temporal correlations in human gamma band electrocorticograms. Electroencephalogr Clin Neurophysiol 98:89–102 (Epub 1996/02/01) CrossRefGoogle Scholar
  31. Mitra P, Bokil H (2008) Observed brain dynamics. Oxford University Press, OxfordGoogle Scholar
  32. Mountcastle VB, Talbot WH, Sakata H, Hyvarinen J (1969) Cortical neuronal mechanisms in flutter-vibration studied in unanesthetized monkeys. Neuronal periodicity and frequency discrimination. J Neurophysiol 32:452–484 (Epub 1969/05/01) CrossRefGoogle Scholar
  33. Muniak MA, Ray S, Hsiao SS, Dammann JF, Bensmaia SJ (2007) The neural coding of stimulus intensity: linking the population response of mechanoreceptive afferents with psychophysical behavior. J Neurosci 27:11687–11699 (Epub 2007/10/26) CrossRefGoogle Scholar
  34. Peng W, Hu L, Zhang Z, Hu Y (2014) Changes of spontaneous oscillatory activity to tonic heat pain. PLoS One 9:e91052 (Epub 2014/03/08) CrossRefGoogle Scholar
  35. Pfurtscheller G, Neuper C, Andrew C, Edlinger G (1997) Foot and hand area mu rhythms. Int J Psychophysiol Jun 26:121–135 (Epub 1997/06/01) CrossRefGoogle Scholar
  36. Pfurtscheller G, Graimann B, Huggins JE, Levine SP, Schuh LA (2003) Spatiotemporal patterns of beta desynchronization and gamma synchronization in corticographic data during self-paced movement. Clin Neurophysiol 114:1226–1236 (Epub 2003/07/05) CrossRefGoogle Scholar
  37. Ray S, Maunsell JH (2011) Different origins of gamma rhythm and high-gamma activity in macaque visual cortex. PLoS Biol 9:e1000610 (Epub 2011/05/03) CrossRefGoogle Scholar
  38. Ray S, Niebur E, Hsiao SS, Sinai A, Crone NE (2008a) High-frequency gamma activity (80–150Hz) is increased in human cortex during selective attention. Clin Neurophysiol 119:116–133 (Epub 2007/11/27) CrossRefGoogle Scholar
  39. Ray S, Hsiao SS, Crone NE, Franaszczuk PJ, Niebur E (2008b) Effect of stimulus intensity on the spike-local field potential relationship in the secondary somatosensory cortex. J Neurosci 28:7334–7343 (Epub 2008/07/18) CrossRefGoogle Scholar
  40. Rossiter HE, Worthen SF, Witton C, Hall SD, Furlong PL (2013) Gamma oscillatory amplitude encodes stimulus intensity in primary somatosensory cortex. Front Hum Neurosci 7:362 (Epub 2013/07/23) CrossRefGoogle Scholar
  41. Ryun S, Kim JS, Jeon E, Chung CK (2017a) Movement-related sensorimotor high-gamma activity mainly represents somatosensory feedback. Front Neurosci 11:408 (Epub 2017/08/05) CrossRefGoogle Scholar
  42. Ryun S, Kim JS, Lee H, Chung CK (2017b) Tactile Frequency-Specific High-Gamma Activities in Human Primary and Secondary Somatosensory Cortices. Sci Rep 7:15442 (Epub 2017/11/15) CrossRefGoogle Scholar
  43. Salinas E, Hernandez A, Zainos A, Romo R (2000) Periodicity and firing rate as candidate neural codes for the frequency of vibrotactile stimuli. J Neurosci 20:5503–5515 (Epub 2000/07/07) CrossRefGoogle Scholar
  44. Schoffelen JM, Poort J, Oostenveld R, Fries P (2011) Selective movement preparation is subserved by selective increases in corticomuscular gamma-band coherence. J Neurosci 31:6750–6758 (Epub 2011/05/06) CrossRefGoogle Scholar
  45. Seeber M, Scherer R, Wagner J, Solis-Escalante T, Muller-Putz GR (2015) High and low gamma EEG oscillations in central sensorimotor areas are conversely modulated during the human gait cycle. Neuroimage 112:318–326 (Epub 2015/03/31) CrossRefGoogle Scholar
  46. Tallon-Baudry C, Bertrand O (1999) Oscillatory gamma activity in humans and its role in object representation. Trends Cogn Sci 3:151–162 (Epub 1999/05/14) CrossRefGoogle Scholar
  47. van Ede F, Szebenyi S, Maris E (2014) Attentional modulations of somatosensory alpha, beta and gamma oscillations dissociate between anticipation and stimulus processing. Neuroimage 97:134–141 (Epub 2014/04/29) CrossRefGoogle Scholar
  48. Wyllie E, Luders H, Morris HH, Lesser RP, Dinner DS, Rothner AD, Erenberg G, Cruse R, Friedman D, Hahn J et al (1988) Subdural electrodes in the evaluation for epilepsy surgery in children and adults. Neuropediatrics 19:80–86 (Epub 1988/05/01) CrossRefGoogle Scholar
  49. Zhang Y, Chen Y, Bressler SL, Ding M (2008) Response preparation and inhibition: the role of the cortical sensorimotor beta rhythm. Neuroscience 156:238–246 (Epub 2008/08/05) CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of NeurosurgeryUniversity of Southern CaliforniaLos AngelesUSA
  2. 2.Department of NeurologyUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Department of Biology and Biological EngineeringCalifornia Institute of TechnologyPasadenaUSA
  4. 4.Tianqiao and Chrissy Chen Brain-machine Interface CenterCalifornia Institute of TechnologyPasadenaUSA
  5. 5.Neurorestoration CenterUniversity of Southern CaliforniaLos AngelesUSA

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