Continuous vs. intermittent neurofeedback to regulate auditory cortex activity of tinnitus patients using real-time fMRI - A pilot study.
The emerging technique of real-time fMRI neurofeedback trains individuals to regulate their own brain activity via feedback from an fMRI measure of neural activity. Optimum feedback presentation has yet to be determined, particularly when working with clinical populations. To this end, we compared continuous against intermittent feedback in subjects with tinnitus. Fourteen participants with tinnitus completed the whole experiment consisting of nine runs (3 runs × 3 days). Prior to the neurofeedback, the target region was localized within the auditory cortex using auditory stimulation (1 kHz tone pulsating at 6 Hz) in an ON-OFF block design. During neurofeedback runs, participants received either continuous (n = 7, age 46.84 ± 12.01, Tinnitus Functional Index (TFI) 49.43 ± 15.70) or intermittent feedback (only after the regulation block) (n = 7, age 47.42 ± 12.39, TFI 49.82 ± 20.28). Participants were asked to decrease auditory cortex activity that was presented to them by a moving bar. In the first and the last session, participants also underwent arterial spin labeling (ASL) and resting-state fMRI imaging. We assessed tinnitus severity using the TFI questionnaire before all sessions, directly after all sessions and six weeks after all sessions. We then compared neuroimaging results from neurofeedback using a general linear model (GLM) and region-of-interest analysis as well as behavior measures employing a repeated-measures ANOVA. In addition, we looked at the seed-based connectivity of the auditory cortex using resting-state data and the cerebral blood flow using ASL data. GLM group analysis revealed that a considerable part of the target region within the auditory cortex was significantly deactivated during neurofeedback. When comparing continuous and intermittent feedback groups, the continuous group showed a stronger deactivation of parts of the target region, specifically the secondary auditory cortex. This result was confirmed in the region-of-interest analysis that showed a significant down-regulation effect for the continuous but not the intermittent group. Additionally, continuous feedback led to a slightly stronger effect over time while intermittent feedback showed best results in the first session. Behaviorally, there was no significant effect on the total TFI score, though on a descriptive level TFI scores tended to decrease after all sessions and in the six weeks follow up in the continuous group. Seed-based connectivity with a fixed-effects analysis revealed that functional connectivity increased over sessions in the posterior cingulate cortex, premotor area and part of the insula when looking at all patients while cerebral blood flow did not change significantly over time. Overall, these results show that continuous feedback is suitable for long-term neurofeedback experiments while intermittent feedback presentation promises good results for single session experiments when using the auditory cortex as a target region. In particular, the down-regulation effect is more pronounced in the secondary auditory cortex, which might be more susceptible to voluntary modulation in comparison to a primary sensory region.
Department of Radiology and Medical Informatics, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland; Medical Image Processing Laboratory, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Campus Biotech, Chemin des Mines 9, Case postale 60, 1211 Geneva 20, Switzerland.
Kirsten
K
Emmert
Department of Radiology and Medical Informatics, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland; Medical Image Processing Laboratory, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Campus Biotech, Chemin des Mines 9, Case postale 60, 1211 Geneva 20, Switzerland.
Rotem
R
Kopel
Department of Radiology and Medical Informatics, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland; Medical Image Processing Laboratory, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Campus Biotech, Chemin des Mines 9, Case postale 60, 1211 Geneva 20, Switzerland; Department of Radiology and Biomedical Imaging, Yale University, 300 Cedar Street, New Haven, CT 06519, USA.
Yury
Y
Koush
Department of ENT, Head & Neck Surgery, Neurotology and Audiology Unit, University Hospital of Lausanne, Rue du Bugnon 21, 1011 Lausanne, Switzerland.
Raphael
R
Maire
Department of Clinical Neurosciences, Service of ORL and HNS, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland.
Pascal
P
Senn
Department of Radiology and Medical Informatics, University Hospitals of Geneva, Rue Gabrielle-Perret-Gentil 4, 1205 Geneva, Switzerland; Medical Image Processing Laboratory, Institute of Bioengineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Campus Biotech, Chemin des Mines 9, Case postale 60, 1211 Geneva 20, Switzerland.
Dimitri
D
Van De Ville
Affidea CDRC - Centre Diagnostique Radiologique de Carouge, Clos de la Fonderie 1, 1227 Carouge, Switzerland; Department of Surgical Sciences, Radiology, Uppsala University, Uppsala, Sweden; Department of Neuroradiology, University Hospital Freiburg, Germany; Faculty of Medicine of the University of Geneva, Switzerland.
Sven
S
Haller
D000328:Adult; D000704:Analysis of Variance; D001303:Auditory Cortex / Q000000981:diagnostic imaging*; D005260:Female; D005500:Follow-Up Studies; D006801:Humans; D007091:Image Processing, Computer-Assisted; D016014:Linear Models; D008279:Magnetic Resonance Imaging; D008297:Male; D008875:Middle Aged; D058765:Neurofeedback / Q000379:methods*; D010100:Oxygen / Q000097:blood; D010865:Pilot Projects; D012146:Rest; D013113:Spin Labels; D011795:Surveys and Questionnaires; D014012:Tinnitus / Q000000981:diagnostic imaging* / Q000534:rehabilitation*
D013113:Spin Labels; D010100:Oxygen
Auditory cortex; Neurofeedback; Real-time fMRI; Self-regulation; Tinnitus