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Religious Chanting and Self-Related Brain Regions: A Multi-Modal Neuroimaging Study

This protocol presents a multi-modal neuroimaging approach to explore the potential brain activity associated with repetitive religious chanting, a ...

University of Bergen

Music is a ubiquitous phenomenon in human cultures, mostly due to its power to evoke and regulate emotions. However, effects of music evoking different emotional experiences such as sadness and happiness on cognition, and in particular on self-generated thought, are unknown. Here we use probe-caught thought sampling and functional magnetic resonance imaging (fMRI) to investigate the influence of sad and happy music on mind-wandering and its underlying neuronal mechanisms. In three experiments we found that sad music, compared with happy music, is associated with stronger mind-wandering (Experiments 1A and 1B) and greater centrality of the nodes of the Default Mode Network (DMN) (Experiment 2). Thus, our results demonstrate that, when listening to sad vs. happy music, people withdraw their attention inwards and engage in spontaneous, self-referential cognitive processes. Importantly, our results also underscore that DMN activity can be modulated as a function of sad and happy music. These findings call for a systematic investigation of the relation between music and thought, having broad implications for the use of music in education and clinical settings.

Effects of Sad and Happy Music on Mind-Wandering and the Default Mode Network.

Sound is a potent elicitor of emotions. Auditory core, belt and parabelt regions have anatomical connections to a large array of limbic and paralimbic structures which are involved in the generation of affective activity. However, little is known about the functional role of auditory cortical regions in emotion processing. Using functional magnetic resonance imaging and music stimuli that evoke joy or fear, our study reveals that anterior and posterior regions of auditory association cortex have emotion-characteristic functional connectivity with limbic/paralimbic (insula, cingulate cortex, and striatum), somatosensory, visual, motor-related, and attentional structures. We found that these regions have remarkably high emotion-characteristic eigenvector centrality, revealing that they have influential positions within emotion-processing brain networks with "small-world" properties. By contrast, primary auditory fields showed surprisingly strong emotion-characteristic functional connectivity with intra-auditory regions. Our findings demonstrate that the auditory cortex hosts regions that are influential within networks underlying the affective processing of auditory information. We anticipate our results to incite research specifying the role of the auditory cortex-and sensory systems in general-in emotion processing, beyond the traditional view that sensory cortices have merely perceptual functions.

The auditory cortex hosts network nodes influential for emotion processing: An fMRI study on music-evoked fear and joy.

Despite extensive research on various types of meditation, research on the neural correlates of religious chanting is in a nascent stage. Using multi-modal electrophysiological and neuroimaging methods, we illustrate that during religious chanting, the posterior cingulate cortex shows the largest decrease in eigenvector centrality, potentially due to regional endogenous generation of delta oscillations. Our data show that these functional effects are not due to peripheral cardiac or respiratory activity, nor due to implicit language processing. Finally, we suggest that the neurophysiological correlates of religious chanting are likely different from those of meditation and prayer, and would possibly induce distinctive psychotherapeutic effects.

The neurophysiological correlates of religious chanting.

Research into hippocampal self-regulation abilities may help determine the clinical significance of hippocampal hyperactivity throughout the pathophysiological continuum of Alzheimer's disease. In this study, we aimed to identify the effects of amyloid-β peptide 42 (amyloid-β42) and phosphorylated tau on the patterns of functional connectomics involved in hippocampal downregulation. We identified 48 cognitively unimpaired participants (22 with elevated CSF amyloid-β peptide 42 levels, 15 with elevated CSF phosphorylated tau levels, mean age of 62.705 ± 4.628 years), from the population-based 'Alzheimer's and Families' study, with baseline MRI, CSF biomarkers, APOE genotyping and neuropsychological evaluation. We developed a closed-loop, real-time functional MRI neurofeedback task with virtual reality and tailored it for training downregulation of hippocampal subfield cornu ammonis 1 (CA1). Neurofeedback performance score, cognitive reserve score, hippocampal volume, number of apolipoprotein ε4 alleles and sex were controlled for as confounds in all cross-sectional analyses. First, using voxel-wise multiple regression analysis and controlling for CSF biomarkers, we identified the effect of healthy ageing on eigenvector centrality, a measure of each voxel's overall influence based on iterative whole-brain connectomics, during hippocampal CA1 downregulation. Then, controlling for age, we identified the effects of abnormal CSF amyloid-β42 and phosphorylated tau levels on eigenvector centrality during hippocampal CA1 downregulation. Across subjects, our main findings during hippocampal downregulation were: (i) in the absence of abnormal biomarkers, age correlated with eigenvector centrality negatively in the insula and midcingulate cortex, and positively in the inferior temporal gyrus; (ii) abnormal CSF amyloid-β42 (<1098) correlated negatively with eigenvector centrality in the anterior cingulate cortex and primary motor cortex; and (iii) abnormal CSF phosphorylated tau levels (>19.2) correlated with eigenvector centrality positively in the ventral striatum, anterior cingulate and somatosensory cortex, and negatively in the precuneus and orbitofrontal cortex. During resting state functional MRI, similar eigenvector centrality patterns in the cingulate had previously been associated to CSF biomarkers in mild cognitive impairment and dementia patients. Using the developed closed-loop paradigm, we observed such patterns, which are characteristic of advanced disease stages, during a much earlier presymptomatic phase. In the absence of CSF biomarkers, our non-invasive, interactive, adaptive and gamified neuroimaging procedure may provide important information for clinical prognosis and monitoring of therapeutic efficacy. We have released the developed paradigm and analysis pipeline as open-source software to facilitate replication studies.

Earliest amyloid and tau deposition modulate the influence of limbic networks during closed-loop hippocampal downregulation.

Neurofeedback training has been shown to influence behavior in healthy participants as well as to alleviate clinical symptoms in neurological, psychosomatic, and psychiatric patient populations. However, many real-time fMRI neurofeedback studies report large inter-individual differences in learning success. The factors that cause this vast variability between participants remain unknown and their identification could enhance treatment success. Thus, here we employed a meta-analytic approach including data from 24 different neurofeedback studies with a total of 401 participants, including 140 patients, to determine whether levels of activity in target brain regions during pretraining functional localizer or no-feedback runs (i.e., self-regulation in the absence of neurofeedback) could predict neurofeedback learning success. We observed a slightly positive correlation between pretraining activity levels during a functional localizer run and neurofeedback learning success, but we were not able to identify common brain-based success predictors across our diverse cohort of studies. Therefore, advances need to be made in finding robust models and measures of general neurofeedback learning, and in increasing the current study database to allow for investigating further factors that might influence neurofeedback learning.

Can we predict real-time fMRI neurofeedback learning success from pretraining brain activity?

During hard times, religious chanting/praying is widely practiced to cope with negative or stressful emotions. While the underlying neural mechanism has not been investigated to a sufficient extent. A previous event-related potential study showed that religious chanting could significantly diminish the late-positive potential induced by negative stimuli. However, the regulatory role of subcortical brain regions, especially the amygdala, in this process remains unclear. This multi-modal MRI study aimed to further clarify the neural mechanism underlying the effectiveness of religious chanting for emotion regulation.

Repetitive Religious Chanting Invokes Positive Emotional Schema to Counterbalance Fear: A Multi-Modal Functional and Structural MRI Study.

Individuals with a predisposition to empathize engage with sad music in a compelling way, experiencing overall more pleasurable emotions. However, the neural mechanisms underlying these music-related experiences in empathic individuals are unknown. The present study tested whether dispositional empathy modulates neural responses to sad compared with happy music. Twenty-four participants underwent fMRI while listening to 4-min blocks of music evoking sadness or happiness. Using voxel-wise regression, we found a positive correlation between trait empathy (with scores assessed by the Interpersonal Reactivity Index) and eigenvector centrality values in the ventromedial prefrontal cortex (vmPFC), including the medial orbitofrontal cortex (mOFC). We then performed a functional connectivity (FC) analysis to detect network nodes showing stronger FC with the vmPFC/mOFC during the presentation of sad versus happy music. By doing so, we identified a "music-empathy" network (vmPFC/mOFC, dorsomedial prefrontal cortex, primary visual cortex, bilateral claustrum and putamen, and cerebellum) that is spontaneously recruited while listening to sad music and includes brain regions that support the coding of compassion, mentalizing, and visual mental imagery. Importantly, our findings extend the current understanding of empathic behaviors to the musical domain and pinpoint sad music as an effective stimulus to be employed in social neuroscience research.

Trait Empathy Shapes Neural Responses Toward Sad Music.

Real-time fMRI neurofeedback is an increasingly popular neuroimaging technique that allows an individual to gain control over his/her own brain signals, which can lead to improvements in behavior in healthy participants as well as to improvements of clinical symptoms in patient populations. However, a considerably large ratio of participants undergoing neurofeedback training do not learn to control their own brain signals and, consequently, do not benefit from neurofeedback interventions, which limits clinical efficacy of neurofeedback interventions. As neurofeedback success varies between studies and participants, it is important to identify factors that might influence neurofeedback success. Here, for the first time, we employed a big data machine learning approach to investigate the influence of 20 different design-specific (e.g. activity vs. connectivity feedback), region of interest-specific (e.g. cortical vs. subcortical) and subject-specific factors (e.g. age) on neurofeedback performance and improvement in 608 participants from 28 independent experiments. With a classification accuracy of 60% (considerably different from chance level), we identified two factors that significantly influenced neurofeedback performance: Both the inclusion of a pre-training no-feedback run before neurofeedback training and neurofeedback training of patients as compared to healthy participants were associated with better neurofeedback performance. The positive effect of pre-training no-feedback runs on neurofeedback performance might be due to the familiarization of participants with the neurofeedback setup and the mental imagery task before neurofeedback training runs. Better performance of patients as compared to healthy participants might be driven by higher motivation of patients, higher ranges for the regulation of dysfunctional brain signals, or a more extensive piloting of clinical experimental paradigms. Due to the large heterogeneity of our dataset, these findings likely generalize across neurofeedback studies, thus providing guidance for designing more efficient neurofeedback studies specifically for improving clinical neurofeedback-based interventions. To facilitate the development of data-driven recommendations for specific design details and subpopulations the field would benefit from stronger engagement in open science research practices and data sharing.

Predictors of real-time fMRI neurofeedback performance and improvement - A machine learning mega-analysis.

Many individuals spend a significant amount of their time "mind-wandering". Mind-wandering often includes spontaneous, nonintentional thought, and a neural correlate of this kind of thought is the default mode network (DMN). Thoughts during mind-wandering can have positive or negative valence, but only little is known about the neural correlates of positive or negative thoughts. We used resting-state functional magnetic resonance imaging (fMRI) and music to evoke mind-wandering in n = 33 participants, with positive-sounding music eliciting thoughts with more positive valence and negative-sounding music eliciting thoughts with more negative valence. Applying purely data-driven analysis methods, we show that medial orbitofrontal cortex (mOFC, part of the ventromedial prefrontal cortex) and the posterior cingulate sulcus (likely area 23c of the posterior cingulate cortex), two sub-regions of the DMN, modulate the valence of thought-contents during mind-wandering. In addition, across two independent experiments, we observed that the posterior cingulate sulcus, a region involved in pain, shows valence-specific functional connectivity with core regions of the brain's putative pain network. Our results suggest that two DMN regions (mOFC and posterior cingulate sulcus) support the formation of negative spontaneous, nonintentional thoughts, and that the interplay between these structures with regions of the putative pain network forms a neural mechanism by which thoughts can become painful.

Tormenting thoughts: The posterior cingulate sulcus of the default mode network regulates valence of thoughts and activity in the brain's pain network during music listening.

Neurofeedback allows for the self-regulation of brain circuits implicated in specific maladaptive behaviors, leading to persistent changes in brain activity and connectivity. Positive-social emotion regulation neurofeedback enhances emotion regulation capabilities, which is critical for reducing the severity of various psychiatric disorders. Training dorsomedial prefrontal cortex (dmPFC) to exert a top-down influence on bilateral amygdala during positive-social emotion regulation progressively (linearly) modulates connectivity within the trained network and induces positive mood. However, the processes during rest that interleave the neurofeedback training remain poorly understood. We hypothesized that short resting periods at the end of training sessions of positive-social emotion regulation neurofeedback would show alterations within emotion regulation and neurofeedback learning networks. We used complementary model-based and data-driven approaches to assess how resting-state connectivity relates to neurofeedback changes at the end of training sessions. In the experimental group, we found lower progressive dmPFC self-inhibition and an increase of connectivity in networks engaged in emotion regulation, neurofeedback learning, visuospatial processing, and memory. Our findings highlight a large-scale synergy between neurofeedback and resting-state brain activity and connectivity changes within the target network and beyond. This work contributes to our understanding of concomitant learning mechanisms post training and facilitates development of efficient neurofeedback training.

Progressive modulation of resting-state brain activity during neurofeedback of positive-social emotion regulation networks.

There is anecdotal evidence for beneficial effects of music therapy in patients with Alzheimer's Disease (AD). However, there is a lack of rigorous research investigating this issue. The aim of this study is to evaluate the effects of music therapy and physical activity on brain plasticity, mood, and cognition in a population with AD and at risk for AD.

Study protocol for the Alzheimer and music therapy study: An RCT to compare the efficacy of music therapy and physical activity on brain plasticity, depressive symptoms, and cognitive decline, in a population with and at risk for Alzheimer's disease.

Statistical learning refers to the implicit mechanism of extracting regularities in our environment. Numerous studies have investigated the neural basis of statistical learning. However, how the brain responds to violations of auditory regularities based on prior (implicit) learning requires further investigation. Here, we used functional magnetic resonance imaging (fMRI) to investigate the neural correlates of processing events that are irregular based on learned local dependencies. A stream of consecutive sound triplets was presented. Unbeknown to the subjects, triplets were either (a) standard, namely triplets ending with a high probability sound or, (b) statistical deviants, namely triplets ending with a low probability sound. Participants (n = 33) underwent a learning phase outside the scanner followed by an fMRI session. Processing of statistical deviants activated a set of regions encompassing the superior temporal gyrus bilaterally, the right deep frontal operculum including lateral orbitofrontal cortex, and the right premotor cortex. Our results demonstrate that the violation of local dependencies within a statistical learning paradigm does not only engage sensory processes, but is instead reminiscent of the activation pattern during the processing of local syntactic structures in music and language, reflecting the online adaptations required for predictive coding in the context of statistical learning.

Brain-correlates of processing local dependencies within a statistical learning paradigm.

This scientific commentary refers to 'Eigenvector centrality dynamics are related to Alzheimer's disease pathological changes in non-demented individuals', by Lorenzini  (https://doi.org/10.1093/braincomms/fcad088).

Eigenvector centrality and its variability over time are promising indicators of alterations in brain function due to early amyloid deposition.

Pain-reducing effects of music listening are well-established, but the effects are small and their clinical relevance questionable. Recent theoretical advances, however, have proposed that synchronizing to music, such as clapping, tapping or dancing, has evolutionarily important social effects that are associated with activation of the endogenous opioid system (which supports both analgesia and social bonding). Thus, active sensorimotor synchronization to music could have stronger analgesic effects than simply listening to music. In this study, we show that sensorimotor synchronization to music significantly amplifies the pain-reducing effects of music listening. Using pressure algometry to the fingernails, pain stimuli were delivered to n = 59 healthy adults either during music listening or silence, while either performing an active tapping task or a passive control task. Compared to silence without tapping, music with tapping (but not simply listening to music) reduced pain with a large, clinically significant, effect size (d = 0.93). Simply tapping without music did not elicit such an effect. Our analyses indicate that both attentional and emotional mechanisms drive the pain-reducing effects of sensorimotor synchronization to music, and that tapping to music in addition to merely listening to music may enhance pain-reducing effects in both clinical contexts and everyday life. The study was registered as a clinical trial at ClinicalTrials.gov (registration number NCT05267795), and the trial was first posted on 04/03/2022.

Sensorimotor synchronization to music reduces pain.

Older age and cognitive inactivity have been associated with cognitive impairment, which in turn is linked to economic and societal burdens due to the high costs of care, especially for care homes and informal care. Emerging non-pharmacological interventions using new technologies, such as virtual reality (VR) delivered on a head-mounted display (HMD), might offer an alternative to maintain or improve cognition. The study aimed to evaluate the efficacy and safety of a VR-based Digital Therapeutics application for improving cognitive functions among healthy older adults.

Virtual reality-based training may improve visual memory and some aspects of sustained attention among healthy older adults - preliminary results of a randomized controlled study.

Article	Year
Effects of Sad and Happy Music on Mind-Wandering and the Default Mode Network. Scientific reports\| PubMed ID: 29089542	2017
The auditory cortex hosts network nodes influential for emotion processing: An fMRI study on music-evoked fear and joy. PloS one\| PubMed ID: 29385142	2018
The neurophysiological correlates of religious chanting. Scientific reports\| PubMed ID: 30862790
Earliest amyloid and tau deposition modulate the influence of limbic networks during closed-loop hippocampal downregulation. Brain : a journal of neurology\| PubMed ID: 32091109	2020
Can we predict real-time fMRI neurofeedback learning success from pretraining brain activity? Human brain mapping\| PubMed ID: 32729652	2020
Repetitive Religious Chanting Invokes Positive Emotional Schema to Counterbalance Fear: A Multi-Modal Functional and Structural MRI Study. Frontiers in behavioral neuroscience\| PubMed ID: 33328917	2020
Trait Empathy Shapes Neural Responses Toward Sad Music. Cognitive, affective & behavioral neuroscience\| PubMed ID: 33474716	2021
Predictors of real-time fMRI neurofeedback performance and improvement - A machine learning mega-analysis. NeuroImage\| PubMed ID: 34048901	2021
Tormenting thoughts: The posterior cingulate sulcus of the default mode network regulates valence of thoughts and activity in the brain's pain network during music listening. Human brain mapping\| PubMed ID: 34652882	2022
Progressive modulation of resting-state brain activity during neurofeedback of positive-social emotion regulation networks. Scientific reports\| PubMed ID: 34862407	2021
Study protocol for the Alzheimer and music therapy study: An RCT to compare the efficacy of music therapy and physical activity on brain plasticity, depressive symptoms, and cognitive declin... PloS one\| PubMed ID: 35771851	2022
Brain-correlates of processing local dependencies within a statistical learning paradigm. Scientific reports\| PubMed ID: 36097186	2022
Eigenvector centrality and its variability over time are promising indicators of alterations in brain function due to early amyloid deposition. Brain communications\| PubMed ID: 37151224	2023
Sensorimotor synchronization to music reduces pain. PloS one\| PubMed ID: 37506059	2023
Virtual reality-based training may improve visual memory and some aspects of sustained attention among healthy older adults - preliminary results of a randomized controlled study. BMC psychiatry\| PubMed ID: 38720251	2024

Stavros Skouras

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