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Research Article

Regulation of the Neural Circuitry of Emotion by Compassion Meditation: Effects of Meditative Expertise

  • Antoine Lutz mail,

    alutz@wisc.edu (AL); rjdavids@wisc.edu (RD)

    Affiliation: University of Wisconsin, Madison, Wisconsin, United States of America

    X
  • Julie Brefczynski-Lewis,

    Affiliation: West Virginia University, Morgantown, West Virginia, United States of America

    X
  • Tom Johnstone,

    Affiliation: University of Reading, Reading, United Kingdom

    X
  • Richard J. Davidson mail

    alutz@wisc.edu (AL); rjdavids@wisc.edu (RD)

    Affiliation: University of Wisconsin, Madison, Wisconsin, United States of America

    X
  • Published: March 26, 2008
  • DOI: 10.1371/journal.pone.0001897

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Referee comments: Referee 2 (Perrine Ruby)

Posted by PLoS_ONE_Group on 27 Mar 2008 at 17:49 GMT

Referee 2's review (Perrine Ruby):

Voluntary regulation of the neural circuitry of emotion by compassion meditation: effects of expertise
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This paper investigated the putative effect of meditation on the cerebral correlates of hearing social emotional sounds. In order to do so the authors measured the BOLD signal (fMRI) during the perception of social emotional sounds (baby laughs, women crying, background noise in a restaurant) when meditating and when resting, both in subjects expert in meditation and in novice subjects (2 X 2 X 3 factorial design : 1st factor = Group, 2nd factor = State, 3rd factor = Valence). Analysis of results revealed a significant effect of meditative practice (Experts vs Novices) on (1) the activity of the brain regions recruited during meditating vs resting, when hearing social sound (i.e. amygdala, temporo-parietal junction), (2) and on the activity of the brain regions responsive to the perception of social emotional sounds (positive/negative vs neutral) during meditation (notably the insula and the somatosensory cortex). This study consequently demonstrates that subjects with the mental expertise to cultivate positive emotion produce different cerebral activity in response to emotional sounds as compared to novice subjects. This strongly suggest that meditation training and practice can influence and then durably modify the brain response to social and emotional stimuli.


This study used an elegant and well controlled design to investigate fascinating issues of putative critical sociocultural consequences : Can we voluntarily modify our brain activity ? can we voluntarily, by active practice, become more empathic and attentive to others by enhancing our cerebral activity in the « social brain circuitry » when perceiving joy or distress in others ?

The challenging design chosen by the authors (investigating the brain of experts in meditation was certainly a real challenge) enabled them to address these issues in an ecological way (expertise in meditation was not experimentally induced) which is quite unusual in affective cognitive neuroscience. This is a great merit of this study.

It is to note that in spite of a quite complicated design, the authors succeeded in presenting very clearly their objective, methods, results and discussion.

I have only minor comments which may provide additional strength to the results and conclusions and possibly improve the presentation of the paper :

Title

To me, the title of the paper is not totally accurate : What subjects voluntarily regulate is their thoughts and emotions during meditation, and not (as far as I know) their brain activity. As a consequence I would recommend a title much more like one of the few proposed below :

Voluntary regulation of emotion by compassion meditation: effects of meditative expertise on the neural circuitry of social cognition

Voluntary regulation of emotion by compassion meditation: which consequences on cerebral functioning ?

Regulation of the neural circuitry of emotion by active practice of compassion meditation

Abbreviations

The authors should add « Ins. » and « PCC » to the list

Results

p.7 : add « OF »
« There were no Group-by-Valence nor State-by-Valence interactions. Voxelwise
analysis of group-by-state interactions showed experts to have had considerably stronger
activation in components of the posterior part OF this network ( .... »

Discussion

Given that the paper submitted:

- used stimuli with social emotions
- rely on results showing that « observing another person's emotional state activates parts of the neuronal network involved in processing that same state in oneself» (p. 4)
- demonstrated an effect of meditative expertise on social emotional sounds perception (positive/negative vs neutral) during meditation in the somatosensory cortex

and that it was shown that the somatosensory cortex is involved in emotional processing (e.g. Adolphs et al. 2000), in first (vs third) person perspective taking (Ruby & Decety, 2001, 2003, 2004), and that this brain region was proposed to play a critical role in Selfhood (Ruby & Legrand 2008), the paper,

Ruby P, Decety J. How would you feel versus how do you think she would feel? A neuroimaging study of perspective-taking with social emotions. J Cogn Neurosci. 2004 Jul-Aug;16(6):988-99.

may be worth mentionning since it shows :

- amygdala activation when imagining social emotions both in 1st and 3rd person perspective,
(I would then add p. 4 and p.9 «Recent fMRI OR PET studies have demonstrated that observing OR IMAGINING another person's emotional state activates parts of the neuronal network involved in processing that same state in oneself, whether it is disgust, (touch), pain, OR SOCIAL EMOTIONS... ». It is to note here that « touch » may not be considered as an emotional state)
- an interaction effect in the somatosensory cortex so that this brain region was found to be more active for Self than Other and even more if in an Emotional context (vs Neutral).
(this result may be interesting to add to the discussion p. 9)

Methods, pupil diameter

p.20 : remove one « that »
« Irrelevant drifts in the pupil diameter data over the course of the scan session were removed by automatically rejecting trials that THAT did not show the average phasic response to sounds. The group analysis was performed on the mean pupil diameter across the first 5
seconds following the end of the sound stimulus. »

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N.B. These are the comments made by the referee when reviewing an earlier version of this paper. Prior to publication the manuscript has been revised in light of these comments and to address other editorial requirements.