Effect of neurofeedback training on auditory evoked potentials’ late components reaction time: a placebo-control study

Ivana  Stanković; Nela V. Ilić; Tihomir V.  Ilić; Ljiljana Jeličić; Mirjana Sovilj; Vesna Martić; Silvana  Punišić; Miodrag Stokić

doi:10.2298/VSP220412072S

Ivana Stanković Institute for Experimental Phonetics and Speech Pathology “Đorđe Kostić”, Belgrade, Serbia
Nela V. Ilić University of Belgrade, Faculty of Medicine, Belgrade, Serbia
Tihomir V. Ilić University of Defence, Faculty of Medicine of the Military Medical Academy, Belgrade, Serbia
Ljiljana Jeličić University Clinical Center of Serbia, Clinic of Physical Medicine and Rehabilitation, Belgrade, Serbia
Mirjana Sovilj Institute for Experimental Phonetics and Speech Pathology “Đorđe Kostić”, Belgrade, Serbia
Vesna Martić University of Defence, Faculty of Medicine of the Military Medical Academy, Belgrade, Serbia
Silvana Punišić Research and Development Institute – Life Activities Advancement Center, Belgrade, Serbia
Miodrag Stokić Educational Center Stokić, Belgrade, Serbia

DOI: https://doi.org/10.2298/VSP220412072S

Keywords: attention, brain, cognition, electroencephalography, event-related potentials, p300, evoked potentials, auditory, feedback, sensory

Abstract

Background/Aim. Neurofeedback (NFB) training of sensorimotor rhythm (SMR) contributes to improving cognitive performance and increasing attention. SMR power is increased when a person is focused and task-oriented. The shorter reaction time (RT) of the P300 auditory evoked potentials (AEPs) is associated with better attention. Hence, the increase in SMR power after NFB SMR training should decrease the RT in a cognitive task. The aim of the study was to examine the ability of healthy individuals to modulate the SMR of electroencephalographic (EEG) activity between 12 and 15 Hz during 20-day NFB training sessions. In addition, the effect of NFB SMR training on RT was investigated. Methods. Participants were divided into experimental and control groups, with 24 subjects (12 males and 12 females) in each group, aged between 25 and 40 years. Participants in the experimental group were trained with authentic NFB SMR training, while in the control group, false (placebo) training was applied. AEPs were registered on five occasions: before NFB training, after 5, 10, and 20 training sessions, and one month after the last training. Results. The results showed that a series of 20 NFB SMR training sessions increased the amplitudes of the SMR. RT in the experimental group was significantly shortened, while in the control group, it was not observed. Moreover, the increase in the power of the EEG signal of the SMR showed a negative correlation with RT, but only in a subgroup of male subjects. Conclusion. The obtained results indicate the effects of NFB training on the improvement of the attention process expressed by RT.

Author Biography

Miodrag Stokić, Educational Center Stokić, Belgrade, Serbia

naučni saradnik

References

1. Campos da Paz VK, Garcia A, Campos da Paz Neto A, Tomaz C. SMR Neurofeedback Training Facilitates Working Memory Performance in Healthy Older Adults: A Behavioral and EEG Study. Front Behav Neurosci 2018; 12: 321.

2. Strehl U, Leins U, Goth G, Klinger C, Hinterberger T, Birbaumer N. Self-regulation of slow cortical potentials: a new treatment for children with attention-deficit/hyperactivity disorder. Pediatrics 2006; 118(5): e1530‒40.

3. Arns M, de Ridder S, Strehl U, Breteler M, Coenen A. Efficacy of neurofeedback treatment in ADHD: the effects on inattention, impulsivity and hyperactivity: a meta-analysis. Clin EEG Neurosci 2009; 40(3): 180‒9.

4. Lee EJ, Jung CH. Additive effects of neurofeedback on the treatment of ADHD: A randomized controlled study. Asian J Psychiatr 2017; 25: 16‒21.

5. Bussalb A, Congedo M, Barthélemy Q, Ojeda D, Acquaviva E, Delorme R, et al. Clinical and Experimental Factors Influencing the Efficacy of Neurofeedback in ADHD: A Meta-Analysis. Front Psychiatry 2019; 10: 35.

6. Qian X, Loo BRY, Castellanos FX, Liu S, Koh HL, Poh XWW, et al. Brain-computer-interface-based intervention re-normalizes brain functional network topology in children with attention deficit/hyperactivity disorder. Transl Psychiatry 2018; 8(1): 149.

7. Sterman MB. Basic concepts and clinical findings in the treatment of seizure disorders with EEG operant conditioning. Clin Electroencephalogr 2000; 31(1): 45‒55.

8. Gruzelier JH. EEG-neurofeedback for optimising performance. I: a review of cognitive and affective outcome in healthy participants. Neurosci Biobehav Rev 2014; 44: 124‒41.

9. Kober SE, Schweiger D, Witte M, Reichert JL, Grieshofer P, Neuper C, et al. Specific effects of EEG based neurofeedback training on memory functions in post-stroke victims. J. Neuroeng Rehabil 2015; 12: 107.

10. Reichert JL, Kober SE, Schweiger D, Grieshofer P, Neuper C, Wood G. Shutting Down Sensorimotor Interferences after Stroke: A Proof-of-Principle SMR Neurofeedback Study. Front Hum Neurosci 2016; 10: 348.

11. Kober SE, Witte M, Stangl M, Valjamae A, Neuper C, Wood G. Shutting down sensorimotor interference unblocks the networks for stimulus processing: an SMR neurofeedback training study. Clin Neurophysiol 2015; 126: 82–95.

12. Hoedlmoser K, Pecherstorfer T, Gruber G, Anderer P, Doppelmayr M, Klimesch W, et al. Instrumental conditioning of human sensorimotor rhythm (12-15 Hz) and its impact on sleep as well as declarative learning. Sleep 2008; 31(10): 1401‒8.

13. Vernon D, Egner T, Cooper N, Compton T, Neilands C, Sheri A, et al. The effect of training distinct neurofeedback protocols on aspects of cognitive performance. Int J Psychophysiol 2003; 47(1): 75‒85.

14. Vernon DJ. Can neurofeedback training enhance performance? An evaluation of the evidence with implications for future research. Appl Psychophysiol Biofeedback 2005; 30(4): 347‒64.

15. Tinius TP, Tinius KA. Changes after EEG biofeedback and cognitive retraining in adults with mild traumatic brain injury and attention deficit hyperactivity disorder. J Neurother 2000; 4: 27–44.

16. Gruzelier J, Egner T, Vernon D. Validating the efficacy of neurofeedback for optimising performance. Prog Brain Res 2006; 159: 421‒31.

17. Autenrieth M, Kober SE, Neuper C, Wood G. How Much Do Strategy Reports Tell About the Outcomes of Neurofeedback Training? A Study on the Voluntary Up-Regulation of the Sensorimotor Rhythm. Front Hum Neurosci 2020; 14: 218.

18. Sitaram R, Ros T, Stoeckel L, Haller S, Scharnowski F, Lewis-Peacock J, et al. Closed-loop brain training: the science of neurofeedback. Nat Rev Neurosci 2017; 18(2): 86‒100.

19. Reiner M, Rozengurt R, Barnea A. Better than sleep: theta neurofeedback training accelerates memory consolidation. Biol Psychol 2014; 95: 45‒53.

20. Zoefel B, Huster RJ, Herrmann CS. Neurofeedback training of the upper alpha frequency band in EEG improves cognitive performance. Neuroimage 2011; 54(2): 1427‒31.

21. Dehghani-Arani F, Rostami R, Nadali H. Neurofeedback training for opiate addiction: Improvement of mental health and craving. Appl Psychophysiol Biofeedback 2013; 38(2): 133‒41.

22. Escolano C, Navarro-Gil M, Garcia-Campayo J, Minguez J. The effects of a single session of upper alpha neurofeedback for cognitive enhancement: A sham-controlled study. Appl Psychophysiol Biofeedback 2014; 39(3‒4): 227‒36.

23. Cheng MY, Huang CJ, Chang YK, Koester D, Schack T, Hung TM, et al. Sensorimotor rhythm neurofeedback enhances golf putting performance. J Sport Exerc Psychol 2015; 37(6): 626‒36.

24. Thompson M, Thompson L. The Neurofeedback Book: An Introduction to Basic Concepts in Applied Psychophysiology Wheat Ridge, CO: Association for Applied Psychophysiology and Biofeedback; 2003.

25. Li H, Li N, Xing Y, Zhang S, Liu C, Cai W, et al. P300 as a Potential Indicator in the Evaluation of Neurocognitive Disorders After Traumatic Brain Injury. Front Neurol 2021; 12: 690792.

26. Frizzo ACF. Auditory evoked potential: a proposal for further evaluation in children with learning disabilities. Front Psychol 2015; 6: 788.

27. Duncan CC, Barry RJ, Connolly JF, Fischer C, Michie PT, Näätänen R, et al. Event-related potentials in clinical research: guidelines for eliciting, recording, and quantifying mismatch negativity, P300, and N400. Clin Neurophysiol 2009; 120(11): 1883‒908.

28. Hasan RA, Reza F, Begum T. Education Level is Associated with Specific N200 and P300 Profiles Reflecting Higher Cognitive Functioning. J Adv Med Pharmacol Sci 2016; 10(4): 1‒12.

29. Lansbergen MM, van Dongen-Boomsma M, Buitelaar JK, Slaats-Willemse D. ADHD and EEG-neurofeedback: a double-blind randomized placebo-controlled feasibility study. J Neural Transm (Vienna) 2011; 118(2): 275‒84.

30. Enriquez-Geppert S, Huster RJ, Herrmann CS. EEG-Neurofeedback as a Tool to Modulate Cognition and Behavior: A Review Tutorial. Front Hum Neurosci 2017; 11: 51.

31. Kober SE, Witte M, Neuper C, Wood G. Specific or nonspecific? Evaluation of band, baseline, and cognitive specificity of sensorimotor rhythm- and gamma-based neurofeedback. Int J Psychophysiol 2017; 120: 1‒13.

32. Gadea M, Aliño M, Hidalgo V, Espert R, Salvador A. Effects of a single session of SMR neurofeedback training on anxiety and cortisol levels. Neurophysiol Clin 2020; 50(3): 167‒73.

33. Doppelmayr M, Weber E. Effects of SMR and Theta/Beta neurofeedback on reaction times, spatial abilities, and creativity. J Neurother 2011; 15(2): 115–29.

34. Gadea M, Aliño M, Garijo E, Espert R, Salvador A. Testing the Benefits of Neurofeedback on Selective Attention Measured Through Dichotic Listening. Appl Psychophysiol Biofeedback 2016; 41(2): 157‒64.

35. Parsaei S, Shetab Bushehri N, Alboghebish S, Rezaeimanesh S, Barati P. Effect of Neurofeedback Training on Improvement of Reaction Time in Elderly, Passive Males. Salmand 2017; 11(4): 550‒7.

36. Duarte JL, Alvarenga KF, Banhara MR, Melo AD, Sás RM, Costa FOA. P300-long-latency auditory evoked potential in normal hearing subjects: simultaneous recording value in Fz and Cz. Braz J Otorhinolaryngol 2009; 75(2): 231‒6.

37. Mohammadi MR, Malmir N, Khaleghi A, Aminiorani M. Comparison of Sensorimotor Rhythm (SMR) and Beta Training on Selective Attention and Symptoms in Children with Attention Deficit/Hyperactivity Disorder (ADHD): A Trend Report. Iran J Psychiatry 2015; 10(3): 165‒74.

38. Au A, Ho GSM, Choi EWM, Leung P, Waye M MY, Kang K, et al. Does it help to train attention in dyslexic children: Pilot case studies with a ten-session neurofeedback program Int J Disabil Hum Dev 2014; 13(1): 45‒54.

39. Bakhshayesh A, Hansch S, Wyschkon A, Rezai M, Esser G. Neuro-feedback in ADHD: a single-blind randomized controlled trial. Eur Child Adolescent Psychiatry 2011; 20: 481–91.

40. Aleagha NF, Naderi F, Heidarei A, Nazari M, Niksirat A, Avakh F. The effect of neurofeedback (smr training) on performance and reaction time of individuals who undertake difficult tasks. Ebnesina 2014; 15(4): 36‒41.

41. Bielas J, Michalczyk Ł. Beta neurofeedback training improves attentional control in the elderly. Psychol Rep 2021; 124(1): 54‒69.

42. Morales-Quezada L, Martinez D, El-Hagrassy MM, Kaptchuk TJ, Sterman MB, Yeh GY. Neurofeedback impacts cognition and quality of life in pediatric focal epilepsy: An exploratory randomized double-blinded sham-controlled trial. Epilepsy Behav 2019; 101(Pt A): 106570.

43. Kaiser DA, Othmer S. Effect of Neurofeedback on Variables of Attention in a Large Multi-Center Trial. J Neuroth 2000; 4(1): 5‒15.

44. Egner T, Gruzelier JH. EEG Biofeedback of low beta band components: Frequency-speciﬁc effects on variables of attention and event-related brain potentials. Clin Neurophysiol 2004; 115(1): 131–9.

45. Adam JJ, Paas FG, Buekers MJ, Wuyts IJ, Spijkers WA, Wallmeyer P. Gender differences in choice reaction time: evidence for differential strategies. Ergonomics 1999; 42(2): 327‒35.

46. Botwinick J, Thompson LW. Components of reaction time in relation to age and sex. J Genet Psychol 1966; 108(2d Half): 175‒83.

47. Dykiert D, Der G, Starr JM, Deary IJ. Sex Differences in Reaction Time Mean and Intraindividual Variability Across the Life Span. Dev Psychol 2012; 48(5): 1262‒76.

48. Ghisletta P, Renaud O, Fagot D, Lecerf T, Ribaupierre A. Age and sex differences in intra-individual variability in a simple reaction time task. Int J Behav Dev 2018; 42(2): 294‒9.

49. Deary IJ, Der G. Reaction Time, Age, and Cognitive Ability: Longitudinal Findings from Age 16 to 63 Years in Representative Population Samples. Aging Neuropsychol Cognit 2005; 12(2): 187–215.