Skip to main content

Advertisement

SpringerLink
Log in

Pearl and pitfalls in brain functional analysis by event-related potentials: a narrative review by the Italian Psychophysiology and Cognitive Neuroscience Society on methodological limits and clinical reliability—part II

  • Review Article
  • Published:
Neurological Sciences Aims and scope Submit manuscript

Abstract

This review focuses on new and/or less standardized event-related potentials methods, in order to improve their knowledge for future clinical applications. The olfactory event-related potentials (OERPs) assess the olfactory functions in time domain, with potential utility in anosmia and degenerative diseases. The transcranial magnetic stimulation-electroencephalography (TMS-EEG) could support the investigation of the intracerebral connections with very high temporal discrimination. Its application in the diagnosis of disorders of consciousness has achieved recent confirmation. Magnetoencephalography (MEG) and event-related fields (ERF) could improve spatial accuracy of scalp signals, with potential large application in pre-surgical study of epileptic patients. Although these techniques have methodological limits, such as high inter- and intraindividual variability and high costs, their diffusion among researchers and clinicians is hopeful, pending their standardization.

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

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kobal G, Hummel T (1994) Olfactory (chemosensory) event-related potentials. Toxicol Ind Health 10:587–596

    CAS  PubMed  Google Scholar 

  2. Landis BN, Negoias S, Friedrich H (2016) Chemosensorisch evozierte Potenziale chemosensory event related potentials. Epileptologie 33:189–196

    Google Scholar 

  3. Kobal G, Plattig KH (1978) Objective olfactometry: methodological annotations for recording olfactory EEG-responses from the awake human. Elektroenzephalogr Elektromyogr Verwandte Geb 9:135–145

    CAS  Google Scholar 

  4. Kobal G (1985) Gustatory evoked potentials in man. Electroencephalogr Clin Neurophysiol Evoked Potentials 62:449–454. https://doi.org/10.1016/0168-5597(85)90055-3

    Article  CAS  PubMed  Google Scholar 

  5. Bonanni E, Borghetti D, Fabbrini M, Maestri M, Cignoni F, Sartucci F (2006) Quantitative EEG analysis in post-traumatic anosmia. Brain Res Bull 71:69–75. https://doi.org/10.1016/j.brainresbull.2006.08.004

    Article  CAS  PubMed  Google Scholar 

  6. Hu B, Han D, Zhang L, Li Y, Zang H, Wang T, Xian M, Zhang W, Yang L, Wang H, He F (2010) Olfactory event-related potential in patients with rhinosinusitis-induced olfactory dysfunction. Am J Rhinol Allergy 24(5):330–335. https://doi.org/10.2500/ajra.2010.24.3517

    Article  PubMed  Google Scholar 

  7. Lötsch J, Hummel T (2006) The clinical significance of electrophysiological measures of olfactory function. Behav Brain Res 170:78–83. https://doi.org/10.1016/j.bbr.2006.02.013

    Article  PubMed  Google Scholar 

  8. Luck SJ (2005). An introduction to event-related potentials and their neural origins. MIT Press, Cambridge, Mass, London

  9. Murphy C, Morgan CD, Geisler MW, Wetter S, Covington JW, Madowitz MD (2000) Olfactory event-related potentials and aging: normative data. Int J Psychophysiol 36:133–145

    CAS  PubMed  Google Scholar 

  10. Rombaux P, Mouraux A, Bertrand B, Guerit J, Hummel T (2006) Assessment of olfactory and trigeminal function using chemosensory event-related potentials. Neurophysiol Clin 36:53–62. https://doi.org/10.1016/j.neucli.2006.03.005

    Article  CAS  PubMed  Google Scholar 

  11. Wang L (2002) The correlation between physiological and psychological responses to odour stimulation in human subjects. Clin Neurophysiol 113:542–551

    PubMed  Google Scholar 

  12. Pause BM, Sojka B, Krauel K, Ferstl R (1996) The nature of the late positive complex within the olfactory event- related potential (OERP). Psychophysiology 33:376–384. https://doi.org/10.1111/j.1469-8986.1996.tb01062.x

    Article  CAS  PubMed  Google Scholar 

  13. Pause BM, Krauel K (2000) Chemosensory event-related potentials (CSERP) as a key to the psychology of odors. Int J Psychophysiol 36:105–122. https://doi.org/10.1016/S0167-8760(99)00105-1

    Article  CAS  PubMed  Google Scholar 

  14. Kettenmann B, Hummel C, Stefan H, Kobal G (1997) Multiple olfactory activity in the human neocortex identified by magnetic source imaging. Chem Senses 22:493–502. https://doi.org/10.1093/chemse/22.5.493

    Article  CAS  PubMed  Google Scholar 

  15. Geisler MW, Murphy C (2000) Event-related brain potentials to attended and ignored olfactory and trigeminal stimuli. Int J Psychophysiol 37:309–315

    CAS  PubMed  Google Scholar 

  16. Picton TW (1992) The P300 wave of the human event-related potential. J Clin Neurophysiol 9:456–479. https://doi.org/10.1097/00004691-199210000-00002

    Article  CAS  PubMed  Google Scholar 

  17. Picton TW (2000) Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. Psychophysiology 37:127–152

    CAS  PubMed  Google Scholar 

  18. Porter J, Anand T, Johnson B, Khan RM, Sobel N (2005) Brain mechanisms for extracting spatial information from smell. Neuron 47:581–592. https://doi.org/10.1016/j.neuron.2005.06.028

    Article  CAS  PubMed  Google Scholar 

  19. Auffermann H, Mathe F, Gerull G, Mrowinski D (1993) Olfactory evoked potentials and contingent negative variation simultaneously recorded for diagnosis of smell disorders. Ann Otol Rhinol Laryngol 102:6–10. https://doi.org/10.1177/000348949310200102

    Article  CAS  PubMed  Google Scholar 

  20. Sirous M, Sinning N, Schneider TR, Friese U, Lorenz J, Engel AK (2019) Chemosensory event-related potentials in response to nasal propylene glycol stimulation. Front Hum Neurosci 13:99. https://doi.org/10.3389/fnhum.2019.00099

    Article  PubMed  PubMed Central  Google Scholar 

  21. Miwa T, Furukawa M, Tsukatani T, Costanzo RM, DiNardo LJ, Reiter ER (2001) Impact of olfactory impairment on quality of life and disability. Arch Otolaryngol Head Neck Surg 127:497–503

    CAS  PubMed  Google Scholar 

  22. Invitto S, Piraino G, Ciccarese V, Carmillo L, Caggiula M, Trianni G (2018) Potential role of OERP as early marker of mild cognitive impairment. Front Aging Neurosci 10:272. https://doi.org/10.3389/fnagi.2018.00272

    Article  PubMed  PubMed Central  Google Scholar 

  23. Lorig TS, Schwartz GE (1988) Brain and odor: I. Alteration of human EEG by odor administration. Psychobiology. https://doi.org/10.3758/BF03327318

  24. Mazzatenta A, Pokorski M, Di Tano A, Cacchio M, Di Giulio C (2016) Influence of sensory stimulation on exhaled volatile organic compounds. Adv Exp Med Biol. https://doi.org/10.1007/5584_2015_176

  25. Morgan CD, Murphy C (2002) Olfactory event-related potentials in Alzheimer’s disease. J Int Neuropsychol Soc 8:753–763

    PubMed  Google Scholar 

  26. Iannilli E, Stephan L, Hummel T, Reichmann H, Haehner A (2017) Olfactory impairment in Parkinson’s disease is a consequence of central nervous system decline. J Neurol 264:1236–1246. https://doi.org/10.1007/s00415-017-8521-0

    Article  PubMed  Google Scholar 

  27. Lorig TS (1989) Human EEG and odor response. Prog Neurobiol 33:387–398

    CAS  PubMed  Google Scholar 

  28. Doty RL (2012) Smell and taste. In: Sinclair AJ, Morley JE, Vellas B (eds) Pathy’s principles and practice of geriatric medicine, Fifth edn. Wiley, p 1061–1072

  29. Malaty J, Malaty IAC (2013) Smell and taste disorders in primary care. Am Fam Physician 88:852–859

  30. Nigri A, Ferraro S, Bruzzone MG, Nava S, D’Incerti L, Bertolino N et al (2016) Central olfactory processing in patients with disorders of consciousness. Eur J Neurol 23:605–612. https://doi.org/10.1111/ene.12907

    Article  CAS  PubMed  Google Scholar 

  31. Croy I, Hummel T (2017) Olfaction as a marker for depression. J Neurol 264:631–638. https://doi.org/10.1007/s00415-016-8227-8

    Article  CAS  PubMed  Google Scholar 

  32. Dileo JF, Brewer WJ, Hopwood M, Anderson V, Creamer M (2008) Olfactory identification dysfunction, aggression and impulsivity in war veterans with post-traumatic stress disorder. Psychol Med 38:523–531. https://doi.org/10.1017/S0033291707001456

    Article  CAS  PubMed  Google Scholar 

  33. Vermetten E, Bremner JD (2003) Olfaction as a traumatic reminder in posttraumatic stress disorder: case reports and review. J Clin Psychiatry 64:202–207. https://doi.org/10.4088/JCP.v64n0214

    Article  PubMed  Google Scholar 

  34. Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL (1999) Olfactory dysfunction in schizophrenia: a qualitative and quantitative review. Neuropsychopharmacology. 21:325–340. https://doi.org/10.1016/S0893-133X(99)00019-6

    Article  CAS  PubMed  Google Scholar 

  35. Stevenson RJ (2013) Olfactory perception, cognition, and dysfunction in humans. Wiley Interdiscip Rev Cogn Sci 4. https://doi.org/10.1002/wcs.1224

  36. Turetsky BI, Hahn CG, Borgmann-Winter K, Moberg PJ (2009) Scents and nonsense: olfactory dysfunction in schizophrenia. Schizophr Bull 35:1117–1131. https://doi.org/10.1093/schbul/sbp111

    Article  PubMed  PubMed Central  Google Scholar 

  37. Olofsson JK, Broman DA, Gilbert PE, Dean P, Nordin S, Murphy C (2006) Laterality of the olfactory event-related potential response:699–704. https://doi.org/10.1093/chemse/bjl011

  38. Frasnelli J, Schuster B, Hummel T (2007) Interactions between olfaction and the trigeminal system: what can be learned from olfactory loss. Cereb Cortex 17:2268–2275

    PubMed  Google Scholar 

  39. Hummel T, Livermore A (2002) Intranasal chemosensory function of the trigeminal nerve and aspects of its relation to olfaction. Int Arch Occup Environ Health 75:305–313

    PubMed  Google Scholar 

  40. Attems J, Walker L, Jellinger KA (2015) Olfaction and aging: a mini-review. Gerontology 61:485–490. https://doi.org/10.1159/000381619

    Article  CAS  PubMed  Google Scholar 

  41. Schriever VA, Góis-Eanes M, Schuster B, Huart C, Hummel T (2014) Olfactory event-related potentials in infants. J Pediatr 165:372–375.e2

    PubMed  Google Scholar 

  42. Brauchli P, Rüegg PB, Etzweiler F, Zeier H (1995) Electrocortical and autonomic alteration by administration of a pleasant and an unpleasant odor. Chem Senses 20:505–515

    CAS  PubMed  Google Scholar 

  43. Martin GN (2013) The neuropsychology of smell and taste. https://doi.org/10.4324/9780203070147

  44. Chaudhury D, Manella L, Arellanos A, Escanilla O, Cleland TA, Linster C (2010) Olfactory bulb habituation to odor stimuli. Behav Neurosci 124:490–499

    PubMed  PubMed Central  Google Scholar 

  45. Poellinger A, Thomas R, Lio P, Lee A, Makris N, Rosen BR, Kwong KK (2001) Activation and habituation in olfaction--an fMRI study. Neuroimage 13:547–560. https://doi.org/10.1006/nimg.2000.0713

    Article  CAS  PubMed  Google Scholar 

  46. Frank RA, Rybalsky K, Brearton M, Mannea E (2011) Odor recognition memory as a function of odor-naming performance. Chem Senses 36:29–41

    PubMed  Google Scholar 

  47. Invitto S, Piraino G, Mignozzi A, Capone S, Montagna G, Siciliano PA et al (2017) Smell and meaning: an OERP study. Smart Innov Syst Technol:289–300. https://doi.org/10.1007/978-3-319-56904-8_28

  48. Invitto S, Mazzatenta A (2019) Olfactory event-related potentials and exhaled organic volatile compounds: the slow link between olfactory perception and breath metabolic response a pilot study on phenylethyl alcohol and vaseline oil. Brain Sci 9:84. https://doi.org/10.3390/brainsci9040084

    Article  CAS  PubMed Central  Google Scholar 

  49. Kobal G, Hummel T (1998) Olfactory and intranasal trigeminal event-related potentials in anosmic patients. Laryngoscope 108:1033–1035

    CAS  PubMed  Google Scholar 

  50. Hummel T, Kaehling C, Grosse F (2016) Automated assessment of intranasal trigeminal function. Rhinology:54. https://doi.org/10.4193/Rhin15.002

  51. Boesveldt S, Haehner A, Berendse HW, Hummel T (2007) Signal-to-noise ratio of chemosensory event-related potentials. Clin Neurophysiol 118:690–695. https://doi.org/10.1016/j.clinph.2006.11.004

    Article  PubMed  Google Scholar 

  52. Invitto S, Calcagnì A, Piraino G, Ciccarese V, Balconi M, De Tommaso M et al (2019) Obstructive sleep apnea syndrome and olfactory perception: an OERP study. Respir Physiol Neurobiol 259:37–44. https://doi.org/10.1016/j.resp.2018.07.002

    Article  PubMed  Google Scholar 

  53. Barker AT, Jalinous R, Freeston IL (1985) Non-invasive magnetic stimulation of human motor cortex. Lancet 1(8437):1106–1107

    CAS  PubMed  Google Scholar 

  54. Ilmoniemi RJ, Kičić D (2010) Methodology for combined TMS and EEG. Brain Topogr 22(4):233–248

    PubMed  Google Scholar 

  55. Amassian VE, Cracco RQ (1987) Human cerebral cortical responses to contralateral transcranial stimulation. Neurosurgery 20(1):148–155

    CAS  PubMed  Google Scholar 

  56. Cracco RQ, Amassian VE, Maccabee PJ, Cracco JB (1989) Comparison of human transcallosal responses evoked by magnetic coil and electrical stimulation. Electroencephalogr Clin Neurophysiol 74:417–424

    CAS  PubMed  Google Scholar 

  57. Ilmoniemi RJ, Virtanen J, Ruohonen J, Karhu J, Aronen HJ, Näätänen R (1997) Neuronal responses to magnetic stimulation reveal cortical reactivity and connectivity. Neuroreport 8:3537–3540

    CAS  PubMed  Google Scholar 

  58. Pellicciari MC, Brignani D, Miniussi C (2013) Excitability modulation of the motor system induced by transcranial direct current stimulation: a multimodal approach. Neuroimage 83:569–580. https://doi.org/10.1016/j.neuroimage.2013.06.076

    Article  PubMed  Google Scholar 

  59. Romero Lauro LJ, Rosanova M, Mattavelli G, Convento S, Pisoni A, Opitz A, Bolognini N, Vallar G (2014) TDCS increases cortical excitability: direct evidence from TMS-EEG. Cortex 58:99–111. https://doi.org/10.1016/j.cortex.2014.05.003

    Article  PubMed  Google Scholar 

  60. Rajji TK, Sun Y, Zomorrodi-Moghaddam R, Farzan F, Blumberger DM, Mulsant BH, Fitzgerald PB, Daskalakis ZJ (2013) PAS-induced potentiation of cortical-evoked activity in the dorsolateral prefrontal cortex. Neuropsychopharmacology 38(12):2545–2552. https://doi.org/10.1038/npp.2013.161

    Article  PubMed  PubMed Central  Google Scholar 

  61. Mattavelli G, Pisoni A, Romero Lauro LJ, Marino BF, Bonomi M, Rosanova M, Papagno C (2019) TMSEEG approach unveils brain mechanisms underlying conscious and unconscious face perception. Brain Stimul 12(4):1010–1019. https://doi.org/10.1016/j.brs.2019.02.022

    Article  PubMed  Google Scholar 

  62. Pisoni A, Romero Lauro LJ, Vergallito A, Maddaluno O, Bolognini N (2018) Cortical dynamics underpinning the self-other distinction of touch: a TMS-EEG study. Neuroimage 178:475–484

    PubMed  Google Scholar 

  63. Casarotto S, Comanducci A, Rosanova M, Sarasso S, Fecchio M, Napolitani M, Pigorini A, G. Casali A, Trimarchi PD, Boly M, Gosseries O, Bodart O, Curto F, Landi C, Mariotti M, Devalle G, Laureys S, Tononi G, Massimini M (2016) Stratification of unresponsive patients by an independently validated index of brain complexity. Ann Neurol 80:718–729

    PubMed  PubMed Central  Google Scholar 

  64. Thut G, Miniussi C (2009) New insights into rhythmic brain activity from TMS–EEG studies. Trends Cogn Sci 13:182–189

    PubMed  Google Scholar 

  65. Thut G, Veniero D, Romei V, Miniussi C, Schyns P, Gross J (2011) Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 21(14):1176–1185. https://doi.org/10.1016/j.cub.2011.05.049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Rosanova M, Casali A, Bellina V, Resta F, Mariotti M, Massimini MJ (2009) Natural frequencies of human corticothalamic circuits. Neurosci 29(24):7679–7685. https://doi.org/10.1523/JNEUROSCI.0445-09.2009

    Article  CAS  Google Scholar 

  67. Bonato C, Miniussi C, Rossini PM (2006) Transcranial magnetic stimulation and cortical evoked potentials: a TMS/EEG co-registration study. Clin Neurophysiol 117:1699–1707

    CAS  PubMed  Google Scholar 

  68. Lioumis P, Kicić D, Savolainen P, Mäkelä JP, Kähkönen S (2009) Reproducibility of TMS-evoked EEG responses. Hum Brain Mapp 30(4):1387–1396. https://doi.org/10.1002/hbm.20608

    Article  PubMed  Google Scholar 

  69. Nikouline V, Ruohonen J, Ilmoniemi RJ (1999) The role of the coil click in TMS assessed with imultaneous. EEG Clin Neurophysiol 110:1325–1328

    CAS  PubMed  Google Scholar 

  70. Tremblay S, Rogasch NC, Premoli I, Blumberger DM, Casarotto S, Chen R (2019) Clinical utility and prospective of TMS–EEG. Clin Neurophysiol 12:4534–4577

    Google Scholar 

  71. Massimini M, Ferrarelli F, Huber R, Esser SK, Singh H, Tononi G (2005) Breakdown of cortical effective connectivity during sleep. Science 309(5744):2228–2232

    CAS  PubMed  Google Scholar 

  72. Premoli I, Castellanos N, Rivolta D, Belardinelli P, Bajo R, Zipser C, Espenhahn S, Heidegger T, Müller-Dahlhaus F, Ziemann U (2014) TMS-EEG signatures of GABAergic neurotransmission in the human cortex. J Neurosci 34:5603–5612

    PubMed  PubMed Central  Google Scholar 

  73. Zanon M, Battaglini PP, Jarmolowska J, Pizzolato G, Busan P (2013) Long-range neural activity evoked by premotor cortex stimulation: a TMS/EEG co-registration study. Front Hum Neurosci 7:803. https://doi.org/10.3389/fnhum.2013.00803

    Article  PubMed  PubMed Central  Google Scholar 

  74. Fecchio M, Pigorini A, Comanducci A, Sarasso S, Casarotto S, Premoli I, Derchi CC, Mazza A, Russo S, Resta F, Ferrarelli F, Mariotti M, Ziemann U, Massimini M, Rosanova (2017) The spectral features of EEG responses to transcranial magnetic stimulation of the primary motor cortex depend on the amplitude of the motor evoked potentials. PLoS One 12(9):e0184910. https://doi.org/10.1371/journal.pone.0184910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Salo VC, Ferrari PF, Fox NA (2019) The role of the motor system in action understanding and communication: evidence from human infants and non-human primates. Dev Psychobiol 61(3):390–401

    PubMed  Google Scholar 

  76. Pisoni A, Mattavelli G, Papagno P, Rosanova M, Casali AG, Romero Lauro LJ (2018) Cognitive enhancement induced by anodal tDCS drives circuit-specific cortical plasticity. Cereb Cortex 28:1132–1140

    PubMed  Google Scholar 

  77. Koch G, Bonnì S, Pellicciari MC, Casula EP, Mancini M, Esposito R, Ponzo V, Picazio S, Di Lorenzo F, Serra L, Motta C, Maiella M, Marra C, Cercignani M, Martorana A, Caltagirone C, Bozzali M (2018) Transcranial magnetic stimulation of the precuneus enhances memory and neural activity in prodromal Alzheimer’s disease. Neuroimage 1(169):302–311. https://doi.org/10.1016/j.neuroimage.2017.12.048

    Article  Google Scholar 

  78. Koch G, Bonnì S, Casula EP, Iosa M, Paolucci S, Pellicciari MC et al (2019) Effect of cerebellar stimulation on gait and balance recovery in patients with hemiparetic stroke: a randomized clinical trial. JAMA Neurol 76:170–178

  79. Zazio A, Bortoletto M, Ruzzoli M, Miniussi C, Veniero D (2019) Perceptual and physiological consequences of dark adaptation: a TMS-EEG study. Brain Topogr 32:773–782. https://doi.org/10.1007/s10548-019-00715-x

    Article  PubMed  Google Scholar 

  80. Bergmann TO, Karabanov A, Hartwigsen G, Thielscher A, Siebner HR (2016) Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: current approaches and future perspectives. Neuroimage 140:4–19

    PubMed  Google Scholar 

  81. Bortoletto M, Veniero D, Thut G, Miniussi C (2015) The contribution of TMS-EEG coregistration in the exploration of the human cortical connectome. Neurosci Biobehav Rev 49:114–124. https://doi.org/10.1016/j.neubiorev.2014.12.014

    Article  PubMed  Google Scholar 

  82. Farzan F, Barr MS, Levinson AJ, Chen R, Wong W, Fitzgerald PB, Daskalakis ZJ (2010) Reliability of long interval cortical inhibition in healthy human subjects: a TMSEEG study. J Neurophysiol 104:1339–1346

    PubMed  Google Scholar 

  83. Koch G, Ponzo V, Di Lorenzo F, Caltagirone C, Veniero D (2013) Hebbian and anti-hebbian spike-timing-dependent plasticity of human cortico-cortical connections. J Neurosci 33:9725–9733

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Casula EP, Pellicciari MC, Picazio S, Caltagirone C, Koch G (2016) Spike-timing-dependent plasticity in the human dorso-lateral prefrontal cortex. Neuroimage 143:204–213

    PubMed  Google Scholar 

  85. Ragazzoni A, Cincotta M, Giovannelli F, Cruse D, Young GB, Miniussi C, Rossi S (2017) Clinical neurophysiology of prolonged disorders of consciousness: from diagnostic stimulation to therapeutic neuromodulation. Clin Neurophysiol 128(9):1629–1646

    PubMed  Google Scholar 

  86. Sun Y, Farzan F, Mulsant BH, Rajji TK, Fitzgerald PB, Barr MS, Downar J, Wong W, Blumberger DM, Daskalakis ZJ (2016) Indicators for remission of suicidal ideation following magnetic seizure therapy in patients with treatment-resistant depression. JAMA Psychiatry 73:337–345

    PubMed  Google Scholar 

  87. Casarotto S, Canali P, Rosanova M, Pigorini A, Fecchio M, Mariotti M, Lucca A, Colombo C, Benedetti F, Massimini M (2013) Assessing the effects of electroconvulsive therapy on cortical excitability by means of transcranial magnetic stimulation and electroencephalography. Brain Topogr 26(2):326–337. https://doi.org/10.1007/s10548-012-0256-8

    Article  PubMed  Google Scholar 

  88. Pellicciari MC, Ponzo V, Caltagirone C, Koch G (2017) Restored asymmetry of prefrontal cortical oscillatory activity after bilateral theta burst stimulation treatment in a patient with major depressive disorder: a TMS-EEG study. Brain Stimul 10:147–149

    PubMed  Google Scholar 

  89. Pellicciari MC, Bonnì S, Ponzo V, Cinnera AM, Mancini M, Casula EP, Sallustio F, Paolucci S, Caltagirone C, Koch G (2018) Dynamic reorganization of TMS-evoked activity in subcortical stroke patients. Neuroimage 175:365–378

    PubMed  Google Scholar 

  90. Bagattini C, Mutanen TP, Fracassi C, Manenti R, Cotelli M, Ilmoniemi RJ, Miniussi C, Bortoletto M (2019) Predicting Alzheimer’s disease severity by means of TMS-EEG coregistration. Neurobiol Aging 80:38–45

    PubMed  Google Scholar 

  91. Mutanen TP, Kukkonen M, Nieminen JO, Stenroos M, Sarvas J, Ilmoniemi RJ (2016) Recovering TMS-evoked EEG responses masked by muscle artifacts. Neuroimage 139:157–166

    PubMed  Google Scholar 

  92. Mutanen TP, Metsomaa J, Liljander S, Ilmoniemi RJ (2018) Automatic and robust noise suppression in EEG and MEG: the SOUND algorithm. Neuroimage 166:135–151

    PubMed  Google Scholar 

  93. Conde V, Tomasevic L, Akopian I, Stanek K, Saturnino GB, Thielscher A, Bergmann TO, Siebner HR (2019) The non-transcranial TMS evoked potential is an inherent source of ambiguity in TMS-EEG studies. Neuroimage 185:300–312

    PubMed  Google Scholar 

  94. Belardinelli P, Biabani M, Blumberger DM, Bortoletto M, Casarotto S, David O, Desideri D, Etkin A, Ferrarelli F, Fitzgerald PB, Fornito A, Gordon PC, Gosseries O, Harquel S, Julkunen P, Keller CJ, Kimiskidis VK, Lioumis P (2019) Reproducibility in TMS-EEG studies: a call for data sharing, standard procedures and effective experimental control. Brain Stimul 12:787–790

    PubMed  Google Scholar 

  95. Siebner HR, Conde V, Tomasevic L, Thielscher A, Bergmann TO (2019) Distilling the essence of TMS-evoked EEG potentials (TEPs): a call for securing mechanistic specificity and experimental rigor. Brain Stimul 12:1051–1054. https://doi.org/10.1016/j.brs.2019.03.076

    Article  PubMed  Google Scholar 

  96. Zrenner C, Belardinelli P, Müller-Dahlhaus F, Ziemann U (2016) Closed-loop neuroscience and non-invasive brain stimulation: a tale of two loops. Front Cell Neurosci 10:92. https://doi.org/10.3389/fncel.2016.00092

    Article  PubMed  PubMed Central  Google Scholar 

  97. Cohen D, Cuffin BN, Yunokuchi K, Maniewski R, Purcell C, Cosgrove GR, Ives J, Kennedy JG, Schomer DL (1990) MEG versus EEG localization test using implanted sources in the human brain. Ann Neurol 28(6):811–817

    CAS  PubMed  Google Scholar 

  98. Baillet S (2017) Magnetoencephalography for brain electrophysiology and imaging. Nat Neurosci 20(3):327–339. https://doi.org/10.1038/nn.4504

    Article  CAS  PubMed  Google Scholar 

  99. Hari R, Puce A, Baillet S, Barnes G, Burgess R, Forss N, Gross J (2018) IFCN-endorsed practical guidelines for clinical magnetoencephalography (MEG). Clin Neurophysiol 129(8):1720–1747. https://doi.org/10.1016/j.clinph.2018.03.042

    Article  PubMed  PubMed Central  Google Scholar 

  100. Parkkonen L (2010) Instrumentation and data preprocessing. In: Hansen C, Peter M, Kringelbach L, Salmelin R (eds) MEG: an introduction to methods. Oxford university press, New York, pp 24–64

    Google Scholar 

  101. Hulten A, Schoffelen J, Udd J, Lam NHL, Hagoort P (2019) NeuroImage How the brain makes sense beyond the processing of single words – an MEG study. Annika Hult 186:586–594. https://doi.org/10.1016/j.neuroimage.2018.11.035

    Article  Google Scholar 

  102. van Es MWJ, Van Schoffelen JS (2019) Stimulus-induced gamma power predicts the amplitude of the subsequent visual evoked response. NeuroImage 186:703–712. https://doi.org/10.1016/j.neuroimage.2018.11.029

    Article  PubMed  Google Scholar 

  103. Näätänen R, Pakarinen S, Rinne T, Takegata R (2004) The mismatch negativity (MMN): towards the optimal paradigm. Clin Neurophysiol 115(1):140–144. https://doi.org/10.1016/j.clinph.2003.04.001

    Article  PubMed  Google Scholar 

  104. Recasens M, Uhlhaas PJ (2017) Test–retest reliability of the magnetic mismatch negativity response to sound duration and omission deviants. NeuroImage 157:184–195. https://doi.org/10.1016/j.neuroimage.2017.05.064

    Article  PubMed  Google Scholar 

  105. Thönnessen H, Zvyagintsev M, Harke KC, Boers F, Dammers J, Norra C, Mathiak K (2008) Optimized mismatch negativity paradigm reflects deficits in schizophrenia patients. A combined EEG and MEG study. Biol Psychol 77(2):205–216. https://doi.org/10.1016/j.biopsycho.2007.10.009

    Article  PubMed  Google Scholar 

  106. Tiitinen H, Alho K, Huotilainen M, Ilmoniemi RJ, Simola J, Näätänen R (1993) Tonotopic auditory cortex and the magnetoencephalographic (MEG) equivalent of the mismatch negativity. Psychophysiology 30(5):537–540

    CAS  PubMed  Google Scholar 

  107. Hsiao FJ, Wu ZA, Ho LT, Lin YY (2009) Theta oscillation during auditory change detection: an MEG study. Biol Psychol 81(1):58–66. https://doi.org/10.1016/j.biopsycho.2009.01.007

    Article  PubMed  Google Scholar 

  108. Rossini PM, Tecchio F, Pizzella V, Lupoi D, Cassetta E, Pasqualetti P, Orlacchio A (1998) On the reorganization of sensory hand areas after mono-hemispheric lesion: a functional (MEG)/anatomical (MRI) integrarive study. Brain Res 782(1–2):153–166. https://doi.org/10.1016/S0006-8993(97)01274-2

    Article  CAS  PubMed  Google Scholar 

  109. Polich J, Kok A (1995) Cognitive and biological determinants of P300: an integrative review. Biol Psychol 41(2):103–146

    CAS  PubMed  Google Scholar 

  110. Polich J (2007) Updating P300: an integrative theory of P3a and P3b. Clin Neurophysiol 118(10):2128–2148. https://doi.org/10.1016/j.clinph.2007.04.019

    Article  PubMed  PubMed Central  Google Scholar 

  111. Mecklinger A, Maess B, Opitz B, Pfeifer E, Cheyne D, Weinberg H (1998) A MEG analysis of the P300 in visual discrimination tasks. Electroencephalogr Clin Neurophysiol Evoked Potent 108(1):45–56. https://doi.org/10.1016/S0168-5597(97)00092-0

    Article  CAS  Google Scholar 

  112. Linden DEJ (2005) The P300: where in the brain is it produced and what does it tell us? Neuroscientist 11(6):563–576. https://doi.org/10.1177/1073858405280524

    Article  CAS  PubMed  Google Scholar 

  113. Bagić AI, Knowlton RC, Rose DF, Ebersole JS (2011) American Clinical Magnetoencephalography Society Clinical Practice Guideline 1: recording and analysis of spontaneous cerebral activity*. J Clin Neurophysiol 28(4):348–354. https://doi.org/10.1097/WNP.0b013e3182272fed

    Article  PubMed  Google Scholar 

  114. Burgess RC, Funke ME, Bowyer SM, Lewine JD, Kirsch HE, Bagić AI (2011) American Clinical Magnetoencephalography Society Clinical Practice Guideline 2: presurgical functional brain mapping using magnetic evoked fields*. J Clin Neurophysiol 28(4):355–361. https://doi.org/10.1097/WNP.0b013e3182272ffe

    Article  PubMed  PubMed Central  Google Scholar 

  115. Hari R, Baillet S, Barnes G, Burgess R, Forss N, Gross J, Taulu S (2018) IFCN-endorsed practical guidelines for clinical magnetoencephalography (MEG). Clin Neurophysiol 129:1720–1747. https://doi.org/10.1016/j.clinph.2018.03.042

    Article  PubMed  PubMed Central  Google Scholar 

  116. Pellegrino G, Hedrich T, Chowdhury R, Hall JA, Lina J, Dubeau F, Grova C (2016) Source localization of the seizure onset zone from ictal EEG / MEG Data. 2546:2528–2546. https://doi.org/10.1002/hbm.23191

  117. Pellegrino G, Hedrich T, Chowdhury RA, Hall JA, Dubeau F, Lina JM, Grova C (2018) Clinical yield of magnetoencephalography distributed source imaging in epilepsy: a comparison with equivalent current dipole method. Hum Brain Mapp 39(1):218–231. https://doi.org/10.1002/hbm.23837

    Article  PubMed  Google Scholar 

  118. Hedrich T, Pellegrino G, Kobayashi E, Lina JM, Grova C (2017) Comparison of the spatial resolution of source imaging techniques in high-density EEG and MEG. NeuroImage 157:531–544. https://doi.org/10.1016/j.neuroimage.2017.06.022

    Article  CAS  PubMed  Google Scholar 

  119. Ottenhausen M, Krieg SM, Meyer B, Ringel F (2015) Functional preoperative and intraoperative mapping and monitoring: increasing safety and efficacy in glioma surgery. 38:1–13. https://doi.org/10.3171/2014.10.FOCUS14611.Disclosure

  120. Frye RE, Rezaie R, Papanicolaou AC (2009) Functional neuroimaging of language using magnetoencephalography. Phys Life Rev 6(1):1–10. https://doi.org/10.1016/j.plrev.2008.08.001

    Article  PubMed  PubMed Central  Google Scholar 

  121. Papanicolaou C, Simos PG, Breier JI, Zouridakis G, Willmore LJ, Wheless JW, Gormley WB (1999) Magnetoencephalographic mapping of the language-specific cortex. J Neurosurg 90(1):85–93. https://doi.org/10.3171/jns.1999.90.1.0085

    Article  CAS  PubMed  Google Scholar 

  122. Pang EW, Wang F, Malone M, Kadis DS, Donner EJ (2011) Localization of Broca’s area using verb generation tasks in the MEG: validation against fMRI. Neurosci Lett 490(3):215–219. https://doi.org/10.1016/j.neulet.2010.12.055

    Article  CAS  PubMed  Google Scholar 

  123. Salmelin R (2007) Clinical neurophysiology of language: the MEG approach. Clin Neurophysiol 118(2):237–254. https://doi.org/10.1016/j.clinph.2006.07.316

    Article  PubMed  Google Scholar 

  124. Betti V, Zappasodi F, Rossini PM, Aglioti SM, Tecchio F (2009) Synchronous with your feelings: sensorimotor {gamma} band and empathy for pain. J Neurosci 29(40):12384–12392. https://doi.org/10.1523/JNEUROSCI.2759-09.2009

    Article  PubMed  PubMed Central  Google Scholar 

  125. Betti V, Della Penna S, de Pasquale F, Mantini D, Marzetti L, Romani GL, Corbetta M (2013) Natural scenes viewing alters the dynamics of functional connectivity in the human brain. Neuron 79(4):782–797. https://doi.org/10.1016/j.neuron.2013.06.022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Pellegrino G, Maran M, Turco C, Weis L, Pino G, Di Piccione F, Arcara G (2018) Bilateral transcranial direct current stimulation reshapes resting-state brain networks: a magnetoencephalography assessment. Neural Plast 2018:2782804. https://doi.org/10.1155/2018/2782804

  127. Sorrentino P, Rucco R, Jacini F, Trojsi F, Lardone A, Baselice F, Sorrentino G (2018) Brain functional networks become more connected as amyotrophic lateral sclerosis progresses: a source level magnetoencephalographic study. NeuroImage 20:564–571. https://doi.org/10.1016/j.nicl.2018.08.001

    Article  PubMed  PubMed Central  Google Scholar 

  128. Paggiaro A, Birbaumer N, Cavinato M, Turco C, Formaggio E, Del Felice A, Piccione F (2016) Magnetoencephalography in stroke recovery and rehabilitation. Front Neurol 7:35

    PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Applied Neurophysiology and Pain Unit-AnpLab-University of Bari Aldo Moro, Bari, Italy

    Marina de Tommaso

  2. Department of Psychology, Sapienza University of Rome, Rome, Italy

    Viviana Betti

  3. Fondazione Santa Lucia, Istituto Di Ricovero e Cura a Carattere Scientifico, Rome, Italy

    Viviana Betti & Giacomo Koch

  4. Dipartimento di Scienze della Salute, University of Milano, Milan, Italy

    Tommaso Bocci

  5. Department of Psychology & NeuroMi, University of Milano Bicocca, Milan, Italy

    Nadia Bolognini

  6. Laboratory of Neuropsychology, IRCCS Istituto Auxologico, Milan, Italy

    Nadia Bolognini

  7. Dept. of Movement, Human and Health Sciences, University of Rome “Foro Italico”, Rome, Italy

    Francesco Di Russo

  8. Department of Human Neuroscience, Sapienza University of Rome, Rome, Italy

    Francesco Fattapposta

  9. Oasi Research Institute -IRCCS, Troina, Italy

    Raffaele Ferri

  10. INSPIRE - Laboratory of Cognitive and Psychophysiological Olfactory Processes, University of Salento, Lecce, Italy

    Sara Invitto

  11. Neuroscience Department, Policlinico Tor Vergata, Rome, Italy

    Giacomo Koch

  12. Center for Mind/Brain Sciences – CIMeC, University of Trento, Rovereto, Italy

    Carlo Miniussi

  13. Cognitive Neuroscience Section, IRCCS Istituto Centro San Giovanni di Dio Fatebenefratelli, Brescia, Italy

    Carlo Miniussi

  14. Brain Imaging and Neural Dynamics Research Group, IRCCS San Camillo Hospital, Venice, Italy

    Francesco Piccione

  15. Unit of Neurology and Clinical Neurophysiology, Fondazione PAS, Scandicci, Florence, Italy

    Aldo Ragazzoni

  16. Section of Neurophysiopathology, Department of Clinical and Experimental Medicine, University of Pisa, Pisa, Italy

    Ferdinando Sartucci

  17. CNR Institute of Neuroscience, Pisa, Italy

    Ferdinando Sartucci

  18. Department of Medicine, Surgery and Neuroscience Siena Brain Investigation and Neuromodulation LAb (SI-BIN Lab), University of Siena, Siena, Italy

    Simone Rossi

  19. Neurology Unit, Bambino Gesù Hospital, Rome, Italy

    Massimiliano Valeriani

  20. Center for Sensory-Motor Interaction, Aalborg University, Aalborg, Denmark

    Massimiliano Valeriani

Authors
  1. Marina de Tommaso
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Viviana Betti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Tommaso Bocci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nadia Bolognini
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesco Di Russo
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Francesco Fattapposta
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Raffaele Ferri
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sara Invitto
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Giacomo Koch
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Carlo Miniussi
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Francesco Piccione
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Aldo Ragazzoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ferdinando Sartucci
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Simone Rossi
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Massimiliano Valeriani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Marina de Tommaso: introduction, manuscript design, and editing

Massimiliano Valeriani: conclusions, manuscript design, and editing

Viviana Betti, Francesco Piccione, Giorgio Arcara, Marco Marino: manuscript editing, event-related field, and magnetoencephalogram chapter

Sara Invitto and Ferdinando Sartucci: manuscript editing, olfactory-evoked potentials chapter

Aldo Ragazzoni: manuscript editing

Francesco Fattapposta: manuscript editing

Raffaele Ferri: manuscript editing

Giacomo Koch: manuscript editing, TMS-EEG chapter

Francesco Di Russo: manuscript editing

Tommaso Bocci: manuscript editing; Carlo Miniussi: manuscript editing;  Nadia Bolognini: manuscript editing; Valentina Bianco: manuscript editing; Marianna Delussi: manuscript editing; Eleonora Gentile: manuscript editing; Fabio Giovannelli: manuscript editing; Daniela Mannarelli: manuscript editing; Elena Mussini: manuscript editing; Caterina Pauletti: manuscript editing; Maria COncetta Pellicciari: manuscript editing; Alberto Pisoni: manuscript editing; Alberto Raggi: manuscript editing

Corresponding author

Correspondence to Massimiliano Valeriani.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Tommaso, M., Betti, V., Bocci, T. et al. Pearl and pitfalls in brain functional analysis by event-related potentials: a narrative review by the Italian Psychophysiology and Cognitive Neuroscience Society on methodological limits and clinical reliability—part II. Neurol Sci 41, 3503–3515 (2020). https://doi.org/10.1007/s10072-020-04527-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10072-020-04527-x

Keywords

Search

Navigation