Advances in fMRI Real-Time Neurofeedback
2017; Elsevier BV; Volume: 21; Issue: 12 Linguagem: Inglês
10.1016/j.tics.2017.09.010
ISSN1879-307X
AutoresTakeo Watanabe, Yuka Sasaki, Kazuhisa Shibata, Mitsuo Kawato,
Tópico(s)EEG and Brain-Computer Interfaces
ResumoAdvanced fMRI neurofeedback can be conducted without participant awareness of what is manipulated. Advanced fMRI neurofeedback techniques use multivariate analysis of a particular brain region to induce a specific activation pattern in the targeted region, rather than simply increasing or decreasing the mean activation level throughout the region. Advanced neurofeedback fMRI techniques can modify connectivity between different brain regions and could lead to amelioration of aberrant connectivity in clinical populations. DecNef integrates aspects such as implicitness, reinforcement schedule with external reward, and multivariate analyses. FCNef integrates aspects such as implicitness, reinforcement schedule with external reward, and connectivity analyses. Functional magnetic resonance imaging (fMRI) neurofeedback is a type of biofeedback in which real-time online fMRI signals are used to self-regulate brain function. Since its advent in 2003 significant progress has been made in fMRI neurofeedback techniques. Specifically, the use of implicit protocols, external rewards, multivariate analysis, and connectivity analysis has allowed neuroscientists to explore a possible causal involvement of modified brain activity in modified behavior. These techniques have also been integrated into groundbreaking new neurofeedback technologies, specifically decoded neurofeedback (DecNef) and functional connectivity-based neurofeedback (FCNef). By modulating neural activity and behavior, DecNef and FCNef have substantially advanced both basic and clinical research. Functional magnetic resonance imaging (fMRI) neurofeedback is a type of biofeedback in which real-time online fMRI signals are used to self-regulate brain function. Since its advent in 2003 significant progress has been made in fMRI neurofeedback techniques. Specifically, the use of implicit protocols, external rewards, multivariate analysis, and connectivity analysis has allowed neuroscientists to explore a possible causal involvement of modified brain activity in modified behavior. These techniques have also been integrated into groundbreaking new neurofeedback technologies, specifically decoded neurofeedback (DecNef) and functional connectivity-based neurofeedback (FCNef). By modulating neural activity and behavior, DecNef and FCNef have substantially advanced both basic and clinical research. Functional magnetic resonance imaging (fMRI; see Glossary) neurofeedback is a type of biofeedback in which real-time online fMRI signals are used to self-regulate brain function [1Birbaumer N. et al.Learned regulation of brain metabolism.Trends Cogn. Sci. 2013; 17: 295-302Abstract Full Text Full Text PDF PubMed Scopus (153) Google Scholar, 2Cox R.W. Jesmanowicz A. Real-time 3D image registration for functional MRI.Magn. Reson. 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Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 13deBettencourt M.T. et al.Closed-loop training of attention with real-time brain imaging.Nat. Neurosci. 2015; 18: 470-475Crossref PubMed Scopus (182) Google Scholar, 14deCharms R.C. et al.Control over brain activation and pain learned by using real-time functional MRI.Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 18626-18631Crossref PubMed Scopus (659) Google Scholar, 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. 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Since its initial development in 2003 [9Weiskopf N. et al.Physiological self-regulation of regional brain activity using real-time functional magnetic resonance imaging (fMRI): methodology and exemplary data.NeuroImage. 2003; 19: 577-586Crossref PubMed Scopus (325) Google Scholar] fMRI neurofeedback research has grown rapidly in popularity. This is demonstrated through the accelerated number of publications on fMRI neurofeedback over the past decades (Figure 1). Such an increase in attention has been accompanied by significant progress in fMRI neurofeedback techniques. We focus on four of these advances. First, the use of implicit protocols allows the participants to be kept unaware of the purpose of neurofeedback training [10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. Behav. 2016; 1: 0006Crossref PubMed Scopus (75) Google Scholar, 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google Scholar] or even the fact that they are being trained [22Ramot M. et al.Covert neurofeedback without awareness shapes cortical network spontaneous connectivity.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: E2413-E2420Crossref PubMed Scopus (45) Google Scholar]. Second, the use of external rewards, such as money, has been reported to facilitate neurofeedback learning [20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 23Sepulveda P. et al.How feedback, motor imagery, and reward influence brain self-regulation using real-time fMRI.Hum. Brain Mapp. 2016; 37: 3153-3171Crossref PubMed Scopus (47) Google Scholar]. Third, the development of multivariate analysis techniques, which allows more sensitive neurofeedback [24Hanson S.J. et al.Combinatorial codes in ventral temporal lobe for object recognition: Haxby (2001) revisited: is there a 'face' area?.NeuroImage. 2004; 23: 156-166Crossref PubMed Scopus (217) Google Scholar, 25Haxby J.V. et al.Distributed and overlapping representations of faces and objects in ventral temporal cortex.Science. 2001; 293: 2425-2430Crossref PubMed Scopus (2717) Google Scholar, 26Haynes J.-D. Rees G. Predicting the orientation of invisible stimuli from activity in human primary visual cortex.Nat. Neurosci. 2005; 8: 686-691Crossref PubMed Scopus (632) Google Scholar, 27Kamitani Y. Tong F. Decoding the visual and subjective contents of the human brain.Nat. Neurosci. 2005; 8: 679-685Crossref PubMed Scopus (1313) Google Scholar, 28Yamashita O. et al.Sparse estimation automatically selects voxels relevant for the decoding of fMRI activity patterns.NeuroImage. 2008; 42: 1414-1429Crossref PubMed Scopus (263) Google Scholar], has been incorporated into neurofeedback [13deBettencourt M.T. et al.Closed-loop training of attention with real-time brain imaging.Nat. Neurosci. 2015; 18: 470-475Crossref PubMed Scopus (182) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 29La Conte S.M. et al.Real-time fMRI using brain-state classification.Hum. Brain Mapp. 2007; 28: 1033-1044Crossref PubMed Scopus (186) Google Scholar]. Fourth, changes of connectivity in a targeted brain network [30Koush Y. et al.Learning control over emotion networks through connectivity-based neurofeedback.Cereb. Cortex. 2017; 27: 1193-1202PubMed Google Scholar, 31Koush Y. et al.Connectivity-based neurofeedback: dynamic causal modeling for real-time fMRI.NeuroImage. 2013; 81: 422-430Crossref PubMed Scopus (117) Google Scholar], which could be a cause of mental abnormalities [32Ichikawa N. et al.Identifying melancholic depression biomarker using whole-brain functional connectivity.arXiv. 2017; (1704.01039)Google Scholar, 33Takagi Y. et al.A neural marker of obsessive-compulsive disorder from whole-brain functional connectivity.Sci. Rep. 2017; 77538Crossref PubMed Scopus (39) Google Scholar, 34Yahata N. et al.A small number of abnormal brain connections predicts adult autism spectrum disorder.Nat. Commun. 2016; 711254Crossref PubMed Scopus (179) Google Scholar], have been incorporated into neurofeedback techniques. Combined, the use of these techniques has provided insights into a causal relationship between the modified neural change and modified behavior. Recently, these four fMRI neurofeedback technique advances have been further integrated into new technological developments, specifically decoded neurofeedback (DecNef), which is usually applied to specific brain regions, and functional connectivity-based neurofeedback (FCNef), which is applied to connectivity strength between different brain regions. Both DecNef and FCNef are recent developments in fMRI neurofeedback techniques with unique features (see below). These technologies have helped uncover the relationships between basic brain functions and behavior, and have successfully been applied in clinical settings (Table 1). Although the results of individual studies using DecNef and FCNef have been promising [10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google Scholar, 35Megumi F. et al.Functional MRI neurofeedback training on connectivity between two regions induces long-lasting changes in intrinsic functional network.Front. Hum. Neurosci. 2015; 9: 160Crossref PubMed Scopus (87) Google Scholar, 36Yamada T. et al.Resting-state functional connectivity-based biomarkers and functional MRI-based neurofeedback for psychiatric disorders: a challenge for developing theranostic biomarkers.Int. J. Neuropsychopharmacol. 2017; 20: 769-781Crossref PubMed Scopus (44) Google Scholar, 37Yamashita A. et al.Connectivity neurofeedback training can differentially change functional connectivity and cognitive performance.Cereb. Cortex. 2017; 27: 4960-4970Crossref PubMed Scopus (43) Google Scholar], several fundamental questions about these technologies have been left unanswered.Table 1Development and Applications of DecNef and FCNef in Chronological OrderYearRefsPopulationMethodTarget brain area/connectivityPurpose of neurofeedback trainingIncrease in neurofeedback scores?Behavioral change?Correlation between neural and behavioral changes?2011Shibata et al. 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google ScholarNormalDecNefEarly visual cortexTo test if inductions of activations in the early visual cortex lead to visual perceptual learning of an orientationYesPerceptual learning of an orientation occurredSignificant(r = 0.87)2015Megumi et al. 35Megumi F. et al.Functional MRI neurofeedback training on connectivity between two regions induces long-lasting changes in intrinsic functional network.Front. Hum. Neurosci. 2015; 9: 160Crossref PubMed Scopus (87) Google ScholarNormalFCNefParietal and motor corticesTo test if FCNef is capable of inducing a long-term increase in target connectivityYesN/AaN/A, not available.N/A2016Amano et al. 10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google ScholarNormalDecNefEarly visual cortexTo test if the early visual cortex is capable of associative learning of an orientation and colorYesAssociative learning of an orientation and red color occurredN/A2016Shibata et al. 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google ScholarNormalDecNefCingulate cortexTo test if induction activations in the cingulate cortex increase and decrease preferences for facesYes for increase and decrease groupsPreferences for faces increased and decreasedSignificant(r = 0.78)2016Koizumi et al. 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. Behav. 2016; 1: 0006Crossref PubMed Scopus (75) Google ScholarNormalDecNefEarly visual cortexTo test if pairings of monetary reward and activations of the early visual cortex lead to counter-conditioning of fear memoryYesSkin conductance response to a fear-associated stimuli decreasedN/A2016Cortese et al.bThe authors published another paper [12] using a different method of data analysis with a different purpose. 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google ScholarNormalDecNefParietal and frontal corticesTo test if inductions of activations in the parietal and frontal cortices increase and decrease perceptual confidenceYes for increase and decrease groupsConfidence in a visual task increased and decreasedSignificant(r = 0.68)2017Taschereau-Dumouchel et al. 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google ScholarPhobiaDecNefVentrotemporal cortexTo test if pairing of monetary reward and activation of the ventrotemporal cortex reduces fear to a specific object categoryYesSkin conductance response to a fearful category decreasedN/A2017Yamada et al. 36Yamada T. et al.Resting-state functional connectivity-based biomarkers and functional MRI-based neurofeedback for psychiatric disorders: a challenge for developing theranostic biomarkers.Int. J. Neuropsychopharmacol. 2017; 20: 769-781Crossref PubMed Scopus (44) Google ScholarMajor depressionFCNefMiddle frontal gyrus and precuneusTo test if FCNef on abnormal connectivity for patients with major depression reduced the severity of depressionYesHamilton depression rating scale improvedSignificant(r = 0.87)2017Yamashita et al. 37Yamashita A. et al.Connectivity neurofeedback training can differentially change functional connectivity and cognitive performance.Cereb. Cortex. 2017; 27: 4960-4970Crossref PubMed Scopus (43) Google ScholarNormalFCNefParietal and motor corticesTo test if changes in target connectivity lead to changes in reaction times in a visual taskYesChanges in reaction times in a color/word Stroop taskSignificant(adjusted R2 = 0.22)a N/A, not available.b The authors published another paper 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar using a different method of data analysis with a different purpose. Open table in a new tab In this review, after briefly discussing each of the four aspects of the recent advances of fMRI neurofeedback, we address the following four questions about recent neurofeedback technologies, specifically DecNef and FCNef. First, how have the four advances (implicitness, reward, multivariate analysis, and connectivity) been integrated into DecNef and FCNef? Second, how do these new technologies control fMRI voxel patterns resulting in specific activity changes at the neuronal level? Third, how is a specific fMRI voxel pattern determined from a huge number of possible combinations of fMRI voxel patterns in a brain region? Fourth, how have these new technologies advanced basic and clinical research? Note that this paper does not aim to comprehensively survey fMRI neurofeedback studies or discuss general models of fMRI neurofeedback. Readers interested in a more comprehensive review of neurofeedback work are encouraged to read other recently published reviews [1Birbaumer N. et al.Learned regulation of brain metabolism.Trends Cogn. Sci. 2013; 17: 295-302Abstract Full Text Full Text PDF PubMed Scopus (153) Google Scholar, 38Marzbani H. et al.Neurofeedback: a comprehensive review on system design, methodology and clinical applications.Basic Clin. Neurosci. 2016; 7: 143-158PubMed Google Scholar, 39Sitaram R. et al.Closed-loop brain training: the science of neurofeedback.Nat. Rev. Neurosci. 2017; 18: 86-100Crossref PubMed Scopus (525) Google Scholar]. We discuss here the characteristics as well as representative basic and clinical studies of each of the above-mentioned four aspects. We indicate how each of these characteristics has an advantage over earlier fMRI neurofeedback studies. Finally, we point out controversies and unclear characteristics of each of these aspects. In conventional fMRI neurofeedback methods, participants are informed of the purpose of training, what the neurofeedback signal represents, what brain function is to be trained by neurofeedback, and/or what behavioral changes are expected to occur [4deCharms R.C. et al.Learned regulation of spatially localized brain activation using real-time fMRI.NeuroImage. 2004; 21: 436-443Crossref PubMed Scopus (264) Google Scholar, 14deCharms R.C. et al.Control over brain activation and pain learned by using real-time functional MRI.Proc. Natl. Acad. Sci. U. S. A. 2005; 102: 18626-18631Crossref PubMed Scopus (659) Google Scholar, 18Scheinost D. et al.Orbitofrontal cortex neurofeedback produces lasting changes in contamination anxiety and resting-state connectivity.Transl. Psychiatry. 2013; 3: e250Crossref PubMed Scopus (119) Google Scholar]. However, recent studies have demonstrated that neurofeedback training can be highly effective even when participants do not know what behavior is being trained, or indeed that they are being trained at all [10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. Behav. 2016; 1: 0006Crossref PubMed Scopus (75) Google Scholar, 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google Scholar, 22Ramot M. et al.Covert neurofeedback without awareness shapes cortical network spontaneous connectivity.Proc. Natl. Acad. Sci. U. S. A. 2016; 113: E2413-E2420Crossref PubMed Scopus (45) Google Scholar]. We have termed this type of fMRI neurofeedback implicit neurofeedback. For example, participants might be presented with a disk that represents their feedback score, and asked to try to make the disk as large as possible without being informed of any additional information. Unknown to the participants, the size of the disk actually reflects the degree of 'similarity' of an fMRI voxel pattern in a specific brain region measured on a real-time basis to the fMRI voxel pattern based on a predetermined targeted neural activity pattern. After repetitive trials with this procedure, participants learn to significantly enhance the degree of the similarity [10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. Behav. 2016; 1: 0006Crossref PubMed Scopus (75) Google Scholar, 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google Scholar]. In other words, they learn to induce neural activity patterns similar to the targeted predetermined activity pattern. Importantly, results of post-experiment questionnaires showed that participants are indeed unaware of what brain functions were being trained [10Amano K. et al.Learning to associate orientation with color in early visual areas by associative decoded fMRI neurofeedback.Curr. Biol. 2016; 26: 1861-1866Abstract Full Text Full Text PDF PubMed Scopus (65) Google Scholar, 11Cortese A. et al.Multivoxel neurofeedback selectively modulates confidence without changing perceptual performance.Nat. Commun. 2016; 713669Crossref PubMed Scopus (82) Google Scholar, 12Cortese A. et al.Decoded fMRI neurofeedback can induce bidirectional confidence changes within single participants.NeuroImage. 2017; 149: 323-337Crossref PubMed Scopus (26) Google Scholar, 15Koizumi A. et al.Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure.Nat. Hum. Behav. 2016; 1: 0006Crossref PubMed Scopus (75) Google Scholar, 19Shibata K. et al.Differential activation patterns in the same brain region led to opposite emotional states.PLoS Biol. 2016; 14: e1002546Crossref PubMed Scopus (44) Google Scholar, 20Shibata K. et al.Perceptual learning incepted by decoded fMRI neurofeedback without stimulus presentation.Science. 2011; 334: 1413-1415Crossref PubMed Scopus (318) Google Scholar, 21Tascereau-Dumouchel V. et al.Towards an unconscious neurotherapy for common fears.bioRxiv. 2017; (Published online July 30, 2017)https://doi.org/10.1101/170183Crossref Google Scholar]. Implicit neurofeedback has several advantages and/or novel features compared to traditional neurofeedback. First, implicit neurofeedback reduces or eliminates the possibility that the changes in brain function or behavior associated with neurofeedback training are due to neural pattern changes involved in the specific intention of the participants to improve the function. This is because, using implicit proposals, participants are aware of the presence of feedback scores, but they are unaware of what the feedback scores represent. Thus, the modified behavior can be more confidently attributed to the brain region that was targeted by the neurofeedback. Second, implicit neurofeedback decreases the possibility of the so-called experimenter effect in which participants consciously or unconsciously learn how to produce results that they think would meet the expectations of the experimenter [40Kennedy J.E. Taddonio J.L. Experimenter effects in parapsychological research.J. Parapsychol. 1976; 40: 1-33Google Scholar] (Box 1). Third, implicit neurofeedback may be applied to clinical interventions where conventional methods do not effectively work. For example, in conventional methodology for extinguishing fear responses to traumatic memories, a participant is repeatedly presented with an aversive stimulus associated with fear [41McNally R.J. Mechanisms of exposure therapy: how neuroscience can improve psychological treatments for anxiety disorders.Clin. Psychol. Rev. 2007; 27: 750-759Crossref PubMed Scopus (240) Google Scholar]. The repeated presentation of the aversive stimulus can cause overwhelming distress in the participant, and can therefore lead to a high dropout rate from the extinction therapy [42Schnurr P.P. et al.Cognitive behavioral therapy for posttraumatic stress disorder in women: a randomized controlled trial.JAMA. 2007; 297: 820-830Crossref PubMed Scopus (659) Google Scholar]. However, the implicitness of neurofeedback could eliminate or greatly reduce the possibility of patients developing such distress during training. Another advantage of implicit feedback in cli
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