Regulation of the neural circuitry of emotion by compassion meditation: effects of meditative expertise

Antoine Lutz, Julie Brefczynski-Lewis, Tom Johnstone, Richard J Davidson, Antoine Lutz, Julie Brefczynski-Lewis, Tom Johnstone, Richard J Davidson

Abstract

Recent brain imaging studies using functional magnetic resonance imaging (fMRI) have implicated insula and anterior cingulate cortices in the empathic response to another's pain. However, virtually nothing is known about the impact of the voluntary generation of compassion on this network. To investigate these questions we assessed brain activity using fMRI while novice and expert meditation practitioners generated a loving-kindness-compassion meditation state. To probe affective reactivity, we presented emotional and neutral sounds during the meditation and comparison periods. Our main hypothesis was that the concern for others cultivated during this form of meditation enhances affective processing, in particular in response to sounds of distress, and that this response to emotional sounds is modulated by the degree of meditation training. The presentation of the emotional sounds was associated with increased pupil diameter and activation of limbic regions (insula and cingulate cortices) during meditation (versus rest). During meditation, activation in insula was greater during presentation of negative sounds than positive or neutral sounds in expert than it was in novice meditators. The strength of activation in insula was also associated with self-reported intensity of the meditation for both groups. These results support the role of the limbic circuitry in emotion sharing. The comparison between meditation vs. rest states between experts and novices also showed increased activation in amygdala, right temporo-parietal junction (TPJ), and right posterior superior temporal sulcus (pSTS) in response to all sounds, suggesting, greater detection of the emotional sounds, and enhanced mentation in response to emotional human vocalizations for experts than novices during meditation. Together these data indicate that the mental expertise to cultivate positive emotion alters the activation of circuitries previously linked to empathy and theory of mind in response to emotional stimuli.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. State by Group by valence…
Figure 1. State by Group by valence Interaction: A.
(AI) and (Ins.) stand for anterior insula and insula, respectively (z = 12 and z = 19, 15 experts and 15 novices, color codes: orange, p

Figure 2. Meditation modulates right insula response…

Figure 2. Meditation modulates right insula response to emotional sounds:

A. Voxel-wise analysis of the…

Figure 2. Meditation modulates right insula response to emotional sounds:
A. Voxel-wise analysis of the Group by State by Valence (negative versus positive sounds) interaction in insula (Ins.) (z = 2, corrected, colors code: orange, p

Figure 3. State by Group Interaction: A.

Figure 3. State by Group Interaction: A.

(Amyg.) stands for amygdala (y = −5, color…

Figure 3. State by Group Interaction: A.
(Amyg.) stands for amygdala (y = −5, color codes: orange, p

Figure 4. Directionality of the brain activation.

Figure 4. Directionality of the brain activation.

Areas showing a negative ( dark blue, p…

Figure 4. Directionality of the brain activation.
Areas showing a negative ( dark blue, p
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References
    1. Brefczynski-Lewis JA, Lutz A, Schaefer HS, Levinson DB, Davidson RJ. Neural correlates of attentional expertise in long-term meditation practitioners. Proc Natl Acad Sci U S A. 2007;104:11483–11488. - PMC - PubMed
    1. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000;97:4398–4403. - PMC - PubMed
    1. Lutz A, Greischar LL, Rawlings NB, Ricard M, Davidson RJ. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:16369–16373. - PMC - PubMed
    1. Gethin R. Oxford: Oxford University Press; 1998. The Foundations of Buddhism.
    1. Dalai Lama X. Boston: Wisdom Publisher; 1995. The world of Tibetan Buddhism: An overview of its philosophy and practice.
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Figure 2. Meditation modulates right insula response…
Figure 2. Meditation modulates right insula response to emotional sounds:
A. Voxel-wise analysis of the Group by State by Valence (negative versus positive sounds) interaction in insula (Ins.) (z = 2, corrected, colors code: orange, p

Figure 3. State by Group Interaction: A.

Figure 3. State by Group Interaction: A.

(Amyg.) stands for amygdala (y = −5, color…

Figure 3. State by Group Interaction: A.
(Amyg.) stands for amygdala (y = −5, color codes: orange, p

Figure 4. Directionality of the brain activation.

Figure 4. Directionality of the brain activation.

Areas showing a negative ( dark blue, p…

Figure 4. Directionality of the brain activation.
Areas showing a negative ( dark blue, p
Similar articles
Cited by
References
    1. Brefczynski-Lewis JA, Lutz A, Schaefer HS, Levinson DB, Davidson RJ. Neural correlates of attentional expertise in long-term meditation practitioners. Proc Natl Acad Sci U S A. 2007;104:11483–11488. - PMC - PubMed
    1. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000;97:4398–4403. - PMC - PubMed
    1. Lutz A, Greischar LL, Rawlings NB, Ricard M, Davidson RJ. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:16369–16373. - PMC - PubMed
    1. Gethin R. Oxford: Oxford University Press; 1998. The Foundations of Buddhism.
    1. Dalai Lama X. Boston: Wisdom Publisher; 1995. The world of Tibetan Buddhism: An overview of its philosophy and practice.
Show all 28 references
Publication types
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Figure 3. State by Group Interaction: A.
Figure 3. State by Group Interaction: A.
(Amyg.) stands for amygdala (y = −5, color codes: orange, p

Figure 4. Directionality of the brain activation.

Figure 4. Directionality of the brain activation.

Areas showing a negative ( dark blue, p…

Figure 4. Directionality of the brain activation.
Areas showing a negative ( dark blue, p
Similar articles
Cited by
References
    1. Brefczynski-Lewis JA, Lutz A, Schaefer HS, Levinson DB, Davidson RJ. Neural correlates of attentional expertise in long-term meditation practitioners. Proc Natl Acad Sci U S A. 2007;104:11483–11488. - PMC - PubMed
    1. Maguire EA, Gadian DG, Johnsrude IS, Good CD, Ashburner J, et al. Navigation-related structural change in the hippocampi of taxi drivers. Proc Natl Acad Sci U S A. 2000;97:4398–4403. - PMC - PubMed
    1. Lutz A, Greischar LL, Rawlings NB, Ricard M, Davidson RJ. Long-term meditators self-induce high-amplitude gamma synchrony during mental practice. Proceedings of the National Academy of Sciences of the United States of America. 2004;101:16369–16373. - PMC - PubMed
    1. Gethin R. Oxford: Oxford University Press; 1998. The Foundations of Buddhism.
    1. Dalai Lama X. Boston: Wisdom Publisher; 1995. The world of Tibetan Buddhism: An overview of its philosophy and practice.
Show all 28 references
Publication types
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Figure 4. Directionality of the brain activation.
Figure 4. Directionality of the brain activation.
Areas showing a negative ( dark blue, p

References

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