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FMRI neurofeedback in the motor system elicits bidirectional changes in activity and in white matter structure in the adult human brain.

ABSTRACT: White matter (WM) plasticity supports skill learning and memory. Up- and downregulation of brain activity in animal models lead to WM alterations. But can bidirectional brain-activity manipulation change WM structure in the adult human brain? We employ fMRI neurofeedback to endogenously and directionally modulate activity in the sensorimotor cortices. Diffusion tensor imaging is acquired before and after two separate conditions, involving regulating sensorimotor activity either up or down using real or sham neurofeedback (n = 20 participants × 4 scans). We report rapid opposing changes in corpus callosum microstructure that depend on the direction of activity modulation. Our findings show that fMRI neurofeedback can be used to endogenously and directionally alter not only brain-activity patterns but also WM pathways connecting the targeted brain areas. The level of associated brain activity in connected areas is therefore a possible mediator of previously described learning-related changes in WM.

SUBMITTER: Sampaio-Baptista C

PROVIDER: S-EPMC8961413 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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fMRI neurofeedback in the motor system elicits bidirectional changes in activity and in white matter structure in the adult human brain.

Sampaio-Baptista Cassandra C Neyedli Heather F HF Sanders Zeena-Britt ZB Diosi Kata K Havard David D Huang YunYing Y Andersson Jesper L R JLR Lühr Michael M Goebel Rainer R Johansen-Berg Heidi H

Cell reports 20211001 4

White matter (WM) plasticity supports skill learning and memory. Up- and downregulation of brain activity in animal models lead to WM alterations. But can bidirectional brain-activity manipulation change WM structure in the adult human brain? We employ fMRI neurofeedback to endogenously and directionally modulate activity in the sensorimotor cortices. Diffusion tensor imaging is acquired before and after two separate conditions, involving regulating sensorimotor activity either up or down using ...[more]

PMID: 34706229

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Project description:Neurofeedback studies using real-time functional magnetic resonance imaging (rt-fMRI) have recently incorporated the multi-voxel pattern decoding approach, allowing for fMRI to serve as a tool to manipulate fine-grained neural activity embedded in voxel patterns. Because of its tremendous potential for clinical applications, certain questions regarding decoded neurofeedback (DecNef) must be addressed. Specifically, can the same participants learn to induce neural patterns in opposite directions in different sessions? If so, how does previous learning affect subsequent induction effectiveness? These questions are critical because neurofeedback effects can last for months, but the short- to mid-term dynamics of such effects are unknown. Here we employed a within-subjects design, where participants underwent two DecNef training sessions to induce behavioural changes of opposing directionality (up or down regulation of perceptual confidence in a visual discrimination task), with the order of training counterbalanced across participants. Behavioral results indicated that the manipulation was strongly influenced by the order and the directionality of neurofeedback training. We applied nonlinear mathematical modeling to parametrize four main consequences of DecNef: main effect of change in confidence, strength of down-regulation of confidence relative to up-regulation, maintenance of learning effects, and anterograde learning interference. Modeling results revealed that DecNef successfully induced bidirectional confidence changes in different sessions within single participants. Furthermore, the effect of up- compared to down-regulation was more prominent, and confidence changes (regardless of the direction) were largely preserved even after a week-long interval. Lastly, the effect of the second session was markedly diminished as compared to the effect of the first session, indicating strong anterograde learning interference. These results are interpreted in the framework of reinforcement learning and provide important implications for its application to basic neuroscience, to occupational and sports training, and to therapy.

Project description:Parkinson's disease (PD) is a movement disorder characterized by the early loss of nigrostriatal dopaminergic pathways producing significant network changes impacting motor coordination. Recently three motor stages of PD have been proposed (a silent period when nigrostriatal loss begins, a prodromal motor period with subtle focal manifestations, and clinical PD) with evidence that motor cortex abnormalities occur to produce clinical PD[8]. We directly assess structural changes in the primary motor cortex and corticospinal tract using parallel analyses of longitudinal clinical and cross-sectional pathological cohorts thought to represent different stages of PD. 18F-FP-CIT positron emission tomography and subtle motor features identified patients with idiopathic rapid-eye-movement sleep behaviour disorder (n = 8) that developed prodromal motor signs of PD. Longitudinal diffusion tensor imaging before and after the development of prodromal motor PD showed higher fractional anisotropy in motor cortex and corticospinal tract compared to controls, indicating adaptive structural changes in motor networks in concert with nigrostriatal dopamine loss. Histological analyses of the white matter underlying the motor cortex showed progressive disorientation of axons with segmental replacement of neurofilaments with α-synuclein, enlargement of myelinating oligodendrocytes and increased density of their precursors. There was no loss of neurons in the motor cortex in early or late pathologically confirmed motor PD compared to controls, although there were early cortical increases in neuronal neurofilament light chain and myelin proteins in association with α-synuclein accumulation. Our results collectively provide evidence of a direct impact of PD on primary motor cortex and its output pathways that begins in the prodromal motor stage of PD with structural changes confirmed in early PD. These adaptive structural changes become considerable as the disease advances potentially contributing to motor PD.

Project description:IntroductionObservational studies have indicated widespread comorbidity of white matter (WM) lesions and Alzheimer's disease (AD) in the elderly, but the causality and direction of their relationship remained unclear. Our study aims to examine the bidirectional causal relationship between WM change and AD using a genetically informed method.MethodsWe performed a bidirectional two-sample mendelian randomization (MR) study to investigate the correlation of three WM phenotypes-white matter hyperintensities (WMH, N = 18,381), fractional anisotropy (FA, N = 17,673), and mean diffusivity (MD, N = 17,467)-with AD (N = 63,926) using summary statistics from genome-wide association studies (GWAS). The inverse variance weighted method (IVW) was used to evaluate the causal estimate and alternative methods to test the heterogeneity, horizontal pleiotropy, and outliers.ResultsThere was no significant causal evidence of WM MRI markers on AD across all MR methods. We identified significant evidence of causal effects of AD on the risk of WMH (OR 1.06, 95% CI 1.03-1.10, p < 0.01). The same direction of effects was observed in MR-Egger, weighted median, and weighted mode analysis. Besides, we also observed a risk causal relationship between AD with MD in MR-Egger, weighted median, and weighted mode-based methods (MR-Egger OR 1.38, 95% CI 1.07-1.79, p = 0.02; weighted median OR 1.21, 95% CI 1.02-1.45, p = 0.03; weighted mode-based OR 1.32, 95% CI 1.14-1.53, p < 0.01). However, the general significance of the causal effect of AD on WMH and MD disappeared when we removed the single nucleotide polymorphisms (SNPs) near the APOE regions, revealing that the ability of AD to increase the risk of white matter damage might be mediated by APOE to some extent. Unfortunately, we did not observe significant causal evidence of AD on FA across all MR analyses.ConclusionsIn this bidirectional MR study, we did not observe that WM injuries were associated with a higher risk of AD. Likewise, genetically predicted AD did not result in a causal effect on white matter damage. However, our research revealed that underlying mechanisms linking AD and white matter lesions might be related to the SNPs near APOE regions.

Project description:Despite the existence of several emotion regulation studies using neurofeedback, interactions among a small number of regions were evaluated, and therefore, further investigation is needed to understand the interactions of the brain regions involved in emotion regulation. We implemented electroencephalography (EEG) neurofeedback with simultaneous functional magnetic resonance imaging (fMRI) using a modified happiness-inducing task through autobiographical memories to upregulate positive emotion. Then, an explorative analysis of whole brain regions was done to understand the effect of neurofeedback on brain activity and the interaction of whole brain regions involved in emotion regulation. The participants in the control and experimental groups were asked to do emotion regulation while viewing positive images of autobiographical memories and getting sham or real (based on alpha asymmetry) EEG neurofeedback, respectively. The proposed multimodal approach quantified the effects of EEG neurofeedback in changing EEG alpha power, fMRI blood oxygenation level-dependent (BOLD) activity of prefrontal, occipital, parietal, and limbic regions (up to 1.9% increase), and functional connectivity in/between prefrontal, parietal, limbic system, and insula in the experimental group. New connectivity links were identified by comparing the brain functional connectivity between experimental conditions (Upregulation and View blocks) and also by comparing the brain connectivity of the experimental and control groups. Psychometric assessments confirmed significant changes in positive and negative mood states in the experimental group by neurofeedback. Based on the exploratory analysis of activity and connectivity among all brain regions involved in emotion regions, we found significant BOLD and functional connectivity increases due to EEG neurofeedback in the experimental group, but no learning effect was observed in the control group. The results reveal several new connections among brain regions as a result of EEG neurofeedback which can be justified according to emotion regulation models and the role of those regions in emotion regulation and recalling positive autobiographical memories.

Dataset Information

FMRI neurofeedback in the motor system elicits bidirectional changes in activity and in white matter structure in the adult human brain.

Publications

fMRI neurofeedback in the motor system elicits bidirectional changes in activity and in white matter structure in the adult human brain.

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