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      Neural shifts in alpha rhythm's dual functioning during empathy maturation

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          Abstract

          Introduction

          Empathy is a social–cognitive process that operates by relying mainly on the suppression of the cortical alpha rhythm. This phenomenon has been evidenced in dozens of electrophysiological studies targeting adult human subjects. Yet, recent neurodevelopmental studies indicated that at a younger age, empathy involves reversed brain responses (e.g., alpha enhancement patterns). In this multimodal study, we capture neural activity at the alpha range, and hemodynamic response and target subjects at approximately 20 years old as a unique time window in development that allows investigating both low‐alpha suppression and high‐alpha enhancement. We aim to further investigate the functional role of low‐alpha power suppression and high‐alpha power enhancement during empathy development.

          Methods

          Brain data from 40 healthy individuals were recorded in two consecutive sessions of magnetoencephalography (MEG) and functional magnetic resonance imaging (fMRI) while subjects perceived vicarious physical pain or no pain.

          Results

          MEG revealed that the alpha pattern shift during empathy happens in an all‐or‐none pattern: power enhancement before 18 and suppression after 18 years of age. Additionally, MEG and fMRI highlight a correspondence between high‐alpha power increase and blood‐oxygen‐level‐dependent (BOLD) decrease before 18, but low‐alpha power decrease and BOLD increase after 18. Importantly, this neurodevelopmental transition was not revealed by four other measures: self‐reported (a) ratings of the task stimuli, (b) ratings of naturalistic vignettes of vicarious pain, (c) trait empathy, or neural data from (d) a control neuroimaging task.

          Discussion

          Findings suggest that at the critical age of around 18, empathy is underpinned by an all‐or‐none transition from high‐alpha power enhancement and functional inhibition to low‐alpha power suppression and functional activation in particular brain regions, possibly indicating a marker of maturation in empathic ability. This work advances a recent neurodevelopmental line of studies and provides insight into the functional maturation of empathy at the coming of age.

          Abstract

          Little is known about the maturational process of empathy. Here, we provide insight into empathy maturation by uncovering a functional transition in neural patterns at the coming of age.

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          Most cited references80

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          Nonparametric statistical testing of EEG- and MEG-data.

          In this paper, we show how ElectroEncephaloGraphic (EEG) and MagnetoEncephaloGraphic (MEG) data can be analyzed statistically using nonparametric techniques. Nonparametric statistical tests offer complete freedom to the user with respect to the test statistic by means of which the experimental conditions are compared. This freedom provides a straightforward way to solve the multiple comparisons problem (MCP) and it allows to incorporate biophysically motivated constraints in the test statistic, which may drastically increase the sensitivity of the statistical test. The paper is written for two audiences: (1) empirical neuroscientists looking for the most appropriate data analysis method, and (2) methodologists interested in the theoretical concepts behind nonparametric statistical tests. For the empirical neuroscientist, a large part of the paper is written in a tutorial-like fashion, enabling neuroscientists to construct their own statistical test, maximizing the sensitivity to the expected effect. And for the methodologist, it is explained why the nonparametric test is formally correct. This means that we formulate a null hypothesis (identical probability distribution in the different experimental conditions) and show that the nonparametric test controls the false alarm rate under this null hypothesis.
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            Measuring individual differences in empathy: Evidence for a multidimensional approach.

            Mark Davis (1983)
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              Event-related EEG/MEG synchronization and desynchronization: basic principles.

              An internally or externally paced event results not only in the generation of an event-related potential (ERP) but also in a change in the ongoing EEG/MEG in form of an event-related desynchronization (ERD) or event-related synchronization (ERS). The ERP on the one side and the ERD/ERS on the other side are different responses of neuronal structures in the brain. While the former is phase-locked, the latter is not phase-locked to the event. The most important difference between both phenomena is that the ERD/ERS is highly frequency band-specific, whereby either the same or different locations on the scalp can display ERD and ERS simultaneously. Quantification of ERD/ERS in time and space is demonstrated on data from a number of movement experiments.
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                Author and article information

                Contributors
                yoniilevy@gmail.com
                Journal
                Brain Behav
                Brain Behav
                10.1002/(ISSN)2157-9032
                BRB3
                Brain and Behavior
                John Wiley and Sons Inc. (Hoboken )
                2162-3279
                18 June 2023
                September 2023
                : 13
                : 9 ( doiID: 10.1002/brb3.v13.9 )
                : e3110
                Affiliations
                [ 1 ] Department of Neuroscience and Biomedical Engineering Aalto University Espoo Finland
                [ 2 ] Baruch Ivcher School of Psychology Reichman University Herzliya Israel
                Author notes
                [*] [* ] Correspondence

                Jonathan Levy, Department of Neuroscience and Biomedical Engineering, Aalto University, Rakentajanaukio 2, 02150 Espoo, Finland.

                Email: yoniilevy@ 123456gmail.com

                Author information
                https://orcid.org/0000-0003-1007-2393
                Article
                BRB33110
                10.1002/brb3.3110
                10498088
                37334437
                9d4b9448-3ed9-4179-a6fe-e2ae5a2008e1
                © 2023 The Authors. Brain and Behavior published by Wiley Periodicals LLC.

                This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 18 May 2023
                : 16 December 2022
                : 19 May 2023
                Page count
                Figures: 8, Tables: 2, Pages: 17, Words: 11235
                Funding
                Funded by: Academy of Finland , doi 10.13039/501100002341;
                Categories
                Registered Report Stage 2
                Registered Report Stage 2
                Custom metadata
                2.0
                September 2023
                Converter:WILEY_ML3GV2_TO_JATSPMC version:6.3.3 mode:remove_FC converted:13.09.2023

                Neurosciences
                alpha rhythm activity,development,neuroscience,pain empathy
                Neurosciences
                alpha rhythm activity, development, neuroscience, pain empathy

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