Neurofeedback in patients with frontal brain lesions: A randomized, controlled double-blind trial

Christine Annaheim, Kerstin Hug, Caroline Stumm, Maya Messerli, Yves Simon, Margret Hund-Georgiadis, Christine Annaheim, Kerstin Hug, Caroline Stumm, Maya Messerli, Yves Simon, Margret Hund-Georgiadis

Abstract

Background: Frontal brain dysfunction is a major challenge in neurorehabilitation. Neurofeedback (NF), as an EEG-based brain training method, is currently applied in a wide spectrum of mental health conditions, including traumatic brain injury.

Objective: This study aimed to explore the capacity of Infra-Low Frequency Neurofeedback (ILF-NF) to promote the recovery of brain function in patients with frontal brain injury.

Materials and methods: Twenty patients hospitalized at a neurorehabilitation clinic in Switzerland with recently acquired, frontal and optionally other brain lesions were randomized to either receive NF or sham-NF. Cognitive improvement was assessed using the Frontal Assessment Battery (FAB) and the Test of Attentional Performance (TAP) tasks regarding intrinsic alertness, phasic alertness and impulse control.

Results: With respect to cognitive improvements, there was no significant difference between the two groups after 20 sessions of either NF or sham-NF. However, in a subgroup of patients with predominantly frontal brain lesions, the improvements measured by the FAB and intrinsic alertness were significantly higher in the NF-group.

Conclusion: This is the first double-blind controlled study using NF in recovery from brain injury, and thus also the first such study of ILF NF. Although the result of the subgroup has limited significance because of the small number of participants, it accentuates the trend seen in the whole group regarding the FAB and intrinsic alertness (p = 0.068, p = 0.079, respectively). We therefore conclude that NF could be a promising candidate promoting the recoveryfrom frontal brain lesions. Further studies with larger numbers of patients and less lesion heterogeneity are needed to verify the usefulness of NF in the neurorehabilitation of patients with frontal brain injury (NCT02957695 ClinicalTrials.gov).

Keywords: brain computer interface; brain recovery; cognitive dysfunction; frontal brain injury; infra-low frequency neurofeedback; neurofeedback (NFB); neurorehabilitation.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Annaheim, Hug, Stumm, Messerli, Simon and Hund-Georgiadis.

Figures

FIGURE 1
FIGURE 1
EEG Electrode Positioning for NF-Training (adapted from: Othmer, 2013).
FIGURE 2
FIGURE 2
Flowchart showing the number of participants and drop-outs during the course of the trial.
FIGURE 3
FIGURE 3
Cognitive improvement in both intervention groups. (A) Frontal Assessment Battery (FAB), (B) TAP intrinsic alertness, (C) TAP phasic alertness, (D) TAP Go/NoGo, n = 20. TAP, Task of Attentional Performance.
FIGURE 4
FIGURE 4
(A–D) Cognitive improvement in the subgroup of patients with mainly frontal brain lesions (FAB), TAP intrinsic alertness, TAP phasic alertness, TAP Go/Nogo, n = 9.

References

    1. Ali J. I., Viczko J., Smart C. M. (2020). Efficacy of neurofeedback interventions for cognitive rehabilitation following brain injury: Systematic review and recommendations for future research. J. Int. Neuropsychol. Soc. 26 31–46. 10.1017/S1355617719001061
    1. Arnould A., Dromer E., Rochat L., Van der Linden M., Azouvi P. (2016). Neurobehavioral and self-awareness changes after traumatic brain injury: Towards new multidimensional approaches. Ann. Phys. Rehabil. Med. 59 18–22. 10.1016/j.rehab.2015.09.002
    1. Arns M., de Ridder S., Strehl U., Breteler M., Coenen A. (2009). Efficacy of neurofeedback treatment in ADHD: The effects on inattention, impulsivity and hyperactivity: A meta-analysis. Clin. EEG Neurosci. 40 180–189. 10.1177/155005940904000311
    1. Arns M., Heinrich H., Strehl U. (2014). Evaluation of neurofeedback in ADHD: The long and winding road. Biol. Psychol. 95 108–115. 10.1016/j.biopsycho.2013.11.013
    1. Becker M., Sturm W., Willmes K., Zimmermann P. (1996). Normierungsstudie zur Aufmerksamkeitstestbatterie (TAP) von Zimmermann, Fimm. Zeitschr. Für Neuropsychol. 9 3–15.
    1. Benke T., Karner E., Delazer M. (2013). FAB-D: German version of the frontal assessment battery. J. Neurol. 260 2066–2072. 10.1007/s00415-013-6929-8
    1. Bertoux M., Funkiewiez A., O’Callaghan C., Dubois B., Hornberger M. (2013). Sensitivity and specificity of ventromedial prefrontal cortex tests in behavioral variant frontotemporal dementia. Alzheimers Dement. 9 S84–S94. 10.1016/j.jalz.2012.09.010
    1. Broyd S. J., Demanuele C., Debener S., Helps S. K., James C. J., Sonuga-Barke E. J. S. (2009). Default-mode brain dysfunction in mental disorders: A systematic review. Neurosci. Biobehav. Rev. 33 279–296.
    1. Buckner R. L., Andrews-Hanna J. R., Schacter D. L. (2008). The brain’s default network: Anatomy, function, and relevance to disease. Ann. N. Y. Acad. Sci. 1124 1–38. 10.1196/annals.1440.011
    1. Chibbaro S., Vallee F., Beccaria K., Poczos P., Makiese O., Fricia M., et al. (2012). Impact de la cranioplastie sur l’hémodynamique cérébrale comme facteur pronostic de l’amélioration clinique chez les patients craniectomisés pour traumatisme crânien grave. Rev. Neurol. (Paris) 1021 91–146. 10.1016/j.neurol.2012.06.016
    1. Cohen J. (1988). Statistical power ANALYSIS for the behavioral sciences. Mahwah, NJ: Lawrence Erlbaum Associates. 10.1016/B978-0-12-179060-8.50012-8
    1. Cortese S., Ferrin M., Brandeis D., Holtmann M., Aggensteiner P., Daley D., et al. (2016). Neurofeedback for attention-deficit/hyperactivity disorder: Meta-analysis of clinical and neuropsychological outcomes from randomized controlled trials. J. Am. Acad. Child Adolesc. Psychiatry 55 444–455. 10.1016/j.jaac.2016.03.007
    1. Dobrushina O. R., Vlasova R. M., Rumshiskaya A. D., Litvinova L. D., Mershina E. A., Sinitsyn V. E., et al. (2020). Modulation of intrinsic brain connectivity by implicit electroencephalographic neurofeedback. Front. Hum. Neurosci. 14:192. 10.3389/fnhum.2020.00192
    1. Dodds T. A., Martin D. P., Stolov W. C., Deyo R. A. (1993). A validation of the functional independence measurement and its performance among rehabilitation inpatients. Arch. Phys. Med. Rehabil. 74 531–536.
    1. Dubois B., Slachevsky A., Litvan I., Pillon B. (2000). The FAB: A frontal assessment battery at bedside. Neurology 55 1621–1626. 10.1212/WNL.55.11.1621
    1. Egner T., Sterman M. B. (2006). Neurofeedback treatment of epilepsy: From basic rationale to practical application. Expert Rev. Neurother. 6 247–257. 10.1586/14737175.6.2.247
    1. Granger C. V., Hamilton B. B., Keith R. A., Zielezny M., Sherwin F. S. (1986). Advances in functional assessment for medical rehabilitation. Top. Geriatr. Rehabil. 1 59–74.
    1. Guevara A. B., Demonet J.-F., Polejaeva E., Knutson K. M., Wassermann E. M., Grafman J., et al. (2016). Association between traumatic brain injury-related brain lesions and long-term caregiver burden. J. Head Trauma Rehabil. 31 1–18. 10.1097/HTR.0000000000000151.Association
    1. Hara Y. (2015). Brain plasticity and rehabilitation in stroke patients. J. Nippon Med. Sch. 82 4–13. 10.1272/jnms.82.4
    1. Harmelech T., Preminger S., Wertman E., Malach R. (2013). The day-after effect: Long term, Hebbian-like restructuring of resting-state fMRI patterns induced by a single epoch of cortical activation. J. Neurosci. 33 9488–9497. 10.1523/JNEUROSCI.5911-12.2013
    1. Hodgson K., Hutchinson A. D., Denson L. (2012). Nonpharmacological treatments for ADHD: A meta-analytic review. J. Atten. Disord. 18 275–282. 10.1177/1087054712444732
    1. Kamiya J. (1968). Conscious control of brain waves. Psychol. Today 1 56–60.
    1. Klauer K. J. (2001). Handbuch kognitives training, 2nd Edn. Göttingen: Verlag für Psychologie Hogrefe.
    1. Kluetsch R. C., Ros T., Théberge J., Frewen P. A., Calhoun V. D., Schmahl C., et al. (2014). Plastic modulation of PTSD resting-state networks and subjective wellbeing by EEG neurofeedback. Acta Psychiatr. Scand. 130 123–136. 10.1111/acps.12229
    1. Koralek A. C., Costa R. M., Carmena J. M. (2013). Temporally precise cell-specific coherence develops in corticostriatal networks during learning. Neuron 79 865–872. 10.1016/j.neuron.2013.06.047
    1. Koralek A. C., Jin X., Long J. D., Costa R. M., Carmena J. M. (2012). Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills. Nature 483 331–335. 10.1038/nature10845
    1. Legarda S. B., Lahti C. E., McDermott D., Michas-Martin A. (2022). Use of novel concussion protocol with infralow frequency neuromodulation demonstrates significant treatment response in patients with persistent postconcussion symptoms, a retrospective study. Front. Hum. Neurosci. 16:894758. 10.3389/fnhum.2022.894758
    1. Malloy P., Grace J. (2005). A review of rating scales for measuring behavior change due to frontal systems damage. Cogn. Behav. Neurol. 18 18–27. 10.1097/01.wnn.0000152232.47901.88
    1. May G., Benson R., Balon R., Boutros N. (2013). Neurofeedback and traumatic brain injury: A literature review. Ann. Clin. Psychiatry 25 289–296.
    1. McAdam D. W., Irwin D. A., Rebert C. S., Knott J. R. (1966). Conative control of the contingent negative variation. Electroencephalogr. Clin. Neurophysiol. 21 194–195. 10.1016/0013-4694(66)90127-1
    1. Megumi F., Yamashita A., Kawato M., Imamizu H. (2015). Functional MRI neurofeedback training on connectivity between two regions induces long-lasting changes in intrinsic functional network. Front. Hum. Neurosci. 9:160. 10.3389/fnhum.2015.00160
    1. Menon V. (2011). Large-scale brain networks and psychopathology: A unifying triple network model. Trends Cogn. Sci. 15 483–506. 10.1016/j.tics.2011.08.003
    1. Micoulaud-Franchi J.-A., McGonigal A., Lopez R., Daudet C., Kotwas I., Bartolomei F. (2015). Electroencephalographic neurofeedback: Level of evidence in mental and brain disorders and suggestions for good clinical practice. Neurophysiol. Clin. 45 423–433. 10.1016/j.neucli.2015.10.077
    1. Monastra V. J., Monastra D. M., George S. (2002). The effects of stimulant therapy, eeg biofeedback, and parenting style on the primary symptoms of attention-deficit/hyperactivity disorder. Appl. Psychophysiol. Biofeedback 27 231–249. 10.1023/a:1021018700609
    1. Nicholson A. A., Rabellino D., Densmore M., Frewen P. A., Paret C., Kluetsch R., et al. (2017). The neurobiology of emotion regulation in posttraumatic stress disorder: Amygdala downregulation via real-time fMRI neurofeedback. Hum. Brain Mapp. 38 541–560. 10.1002/hbm.23402
    1. Nicholson A. A., Ros T., Frewen P. A., Densmore M., Théberge J., Kluetsch R. C., et al. (2016). Alpha oscillation neurofeedback modulates amygdala complex connectivity and arousal in posttraumatic stress disorder. Neuroimage Clin. 12 506–516. 10.1016/j.nicl.2016.07.006
    1. Othmer S. F. (2013). Protokoll leitfaden, 4th Editio Edn. Los Angeles, CA: EEG Info Publications.
    1. Othmer S., Othmer S. F., Kaiser D. A., Putman J. (2013). Endogenous neuromodulation at infralow frequencies. Semin. Pediatr. Neurol. 20 246–257. 10.1016/j.spen.2013.10.006
    1. Ottenbacher K. J., Hsu Y., Granger C. V., Fiedler R. C. (1996). The reliability of the functional independence measure: A quantitative review. Arch. Phys. Med. Rehabil. 77 1226–1232. 10.1016/s0003-9993(96)90184-7
    1. Peniston E. G., Kulkosky P. J. (1991). Alpha-theta brainwave neuro-feedback for vietnam veterans with combat- related post-traumatic stress disorder. Med. Psychother. 4 47–60.
    1. Prigatano G. P. (2005). Disturbances of self-awareness and rehabilitation of patients with traumatic brain injury: A 20-year perspective. J. Head Trauma Rehabil. 20 19–29. 10.1097/00001199-200501000-00004
    1. Riesco-Matías P., Yela-Bernabé J. R., Crego A., Sánchez-Zaballos E. (2019). What do meta-analyses have to say about the efficacy of neurofeedback applied to children with ADHD? Review of previous meta-analyses and a new meta-analysis. J. Atten. Disord. 25, 473–485. 10.1177/1087054718821731
    1. Rogala J., Jurewicz K., Paluch K., Kublik E., Cetnarski R., Wróbel A. (2016). The do’s and don’ts of neurofeedback training: A review of the controlled studies using healthy adults. Front. Hum. Neurosci. 10:301. 10.3389/fnhum.2016.00301
    1. Rossini P. M., Altamura C., Ferreri F., Melgari J. M., Tecchio F., Tombini M., et al. (2007). Neuroimaging experimental studies on brain plasticity in recovery from stroke. Eur. Medicophys. 43 241–254.
    1. Roth S. R., Sterman M. B., Clemente C. D. (1967). Comparison of EEG correlates of reinforcement, internal inhibition and sleep. Electroencephalogr. Clin. Neurophysiol. 23 509–520. 10.1016/0013-4694(67)90017-x
    1. Scott W., Kaiser D., Othmer S., Sideroff S. (2005). Effects of an EEG biofeedback protocol on a mixed substance abusing population. Am. J. Drug Alcohol Abus. 31 455–469. 10.1081/ada-200056807
    1. Sitaram R., Ros T., Stoeckel L., Haller S., Scharnowski F., Lewis-Peacock J., et al. (2017). Closed-loop brain training: The science of neurofeedback. Nat. Rev. Neurosci. 18 86–100. 10.1038/nrn.2016.164
    1. Sonuga-Barke E. J. S., Brandeis D., Cortese S., Daley D., Ferrin M., Holtmann M., et al. (2013). Nonpharmacological interventions for ADHD: Systematic review and meta-analyses of randomized controlled trials of dietary and psychological treatments. Am. J. Psychiatry 170 275–289. 10.1176/appi.ajp.2012.12070991
    1. Sterman M. B., Friar L. (1972). Suppression of seizures in an epileptic following sensorimotor EEG feedback training. Electroencephalogr. Clin. Neurophysiol. 33 89–95. 10.1016/0013-4694(72)90028-4
    1. Sterman M. B., Wyrwicka W., Howe R. (1969). Behavioral and neurophysiological studies of the sensorimotor rhythm in the cat. Electroencephalogr. Clin. Neurophysiol. 27 678–679. 10.1016/0013-4694(69)91281-4
    1. Uchida S., Kawashima R. (2008). Reading and solving arithmetic problems improves cognitive functions of normal aged people: A randomized controlled study. Age (Dordr) 30 21–29. 10.1007/s11357-007-9044-x
    1. van der Kolk B. A., Hodgdon H., Gapen M., Musicaro R., Suvak M. K., Hamlin E., et al. (2016). A randomized controlled study of neurofeedback for chronic PTSD. PLoS One 11:e0166752. 10.1371/journal.pone.0166752
    1. Van Doren J., Arns M., Heinrich H., Vollebregt M. A., Strehl U., Loo S. K. (2019). Sustained effects of neurofeedback in ADHD: A systematic review and meta-analysis. Eur. Child Adolesc. Psychiatry 28 293–305. 10.1007/s00787-018-1121-4
    1. Wells R., Dywan J., Dumas J. (2005). Life satisfaction and distress in family caregivers as related to specific behavioural changes after traumatic brain injury. Brain Inj. 19 1105–1115. 10.1080/02699050500150062
    1. World Medical Association (2013). World medical association declaration of Helsinki: Ethical principles for medical research involving human subjects world medical association declaration of Helsinki special communication. JAMA 310 2191–2194. 10.1001/jama.2013.281053
    1. Zimmermann P., Fimm B. (2007). Testbatterie zur aufmerksamkeitsprüfung-version 2.1:(TAP). Herzogenrath: Psytest.

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