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- Publisher
- Springer Journals
- Copyright
- Copyright © 2013 by Melloni et al.; licensee BioMed Central Ltd.
- Subject
- Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
- eISSN
- 1744-9081
- DOI
- 10.1186/1744-9081-9-47
- pmid
- 24365106
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Abstract
Background: Interoception refers to the conscious perception of body signals. Mindfulness is a meditation practice that encourages individuals to focus on their internal experiences such as bodily sensations, thoughts, and emotions. In this study, we selected a behavioral measure of interoceptive sensitivity (heartbeat detection task, HBD) to compare the effect of meditation practice on interoceptive sensitivity among long term practitioners (LTP), short term meditators (STM, subjects that completed a Mindfulness-Based Stress Reduction (MBSR) program) and controls (non-meditators). All participants were examined with a battery of different tasks including mood state, executive function and social cognition tests (emotion recognition, empathy and theory of mind). Findings: Compared to controls, both meditators’ groups showed lower levels of anxiety and depression, but no improvement in executive function or social cognition performance was observed (except for lower scores compared to controls only in the personal distress dimension of empathy). More importantly, meditators’ performance did not differ from that of nonmeditators regarding cardiac interoceptive sensitivity. Conclusion: Results suggest no influence of meditation practice in cardiac interoception and in most related social cognition measures. These negative results could be partially due to the fact that awareness of heartbeat sensations is not emphasized during mindfulness/vipassana meditation and may not be the best index of the awareness supported by the practice of meditation. Keywords: Interoception, Meditation, Mindfulness, Social cognition, Heartbeat detection task Background One component of meditation involves the development Interoception involves the conscious perception of of interoceptive attention to visceral sensations [7]. Add- feelings from inside the body [1-3]. Interoception has been itionally, meditation practice promotes the development proposed to modulate social cognition processes such as of prosocial behavior [8]. motivational behavior [2], empathy [4], and theory of Previous findings reported no difference in interocep- mind (ToM), which have been suggested to be supported tion accuracy between meditators and nonmeditators by emotional and body feedback information [4]. [5,9]. In these studies, a heartbeat discrimination paradigm Meditation is a form of mental training [5] encour- was selected: participants had to discriminate whether aging individuals to focus on their internal experiences, their heartbeats synchronized with either auditory or such as bodily sensations, thoughts, and emotions [6]. visual cues [10]. Consequently, subjects had to attend at the same time to their cardiac sensation and to external stimuli which have been shown to affect interoceptive * Correspondence: aibanez@ineco.org.ar performance [11]. We selected a different heartbeat detec- Laboratory of Experimental Psychology and Neuroscience (LPEN), INECO (Institute of Cognitive Neurology) and Institute of Neuroscience, Favaloro, tion paradigm [12] to avoid the possible interference of Favaloro University, C1078AAI, Buenos Aires, Argentina external stimuli. Moreover, given the relationship between UDP-INECO Foundation Core on Neuroscience (UIFCoN), Diego Portales interoception and social cognition [2,4,13,14], we included University, Santiago, Chile Full list of author information is available at the end of the article © 2013 Melloni et al.; licensee BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Melloni et al. Behavioral and Brain Functions 2013, 9:47 Page 2 of 6 http://www.behavioralandbrainfunctions.com/content/9/1/47 tasks of emotion recognition, empathy and ToM to test Neuropsychological and clinical evaluation the association among bodily perception, social cognition Participants completed the Beck’s Depression Inventory and meditation practice. Moreover, considering the inter- (BDI) and the State Trait Anxiety Inventory (STAI) to action between executive functions (EF) and social cog- evaluate mood and affective state, respectively. EF were nition domains (emotional processing [15], ToM [16] and assessed with the INECO Frontal Screening (IFS) [19] empathy [17]), EF abilities were also evaluated. indexing 8 EF (see Additional file 1: Table S1) and the Our aim was to compare the effect of meditation prac- Stroop test. tice on interoceptive sensitivity and related measures among long term practitioners (LTP), subjects that Social cognition tasks completed a Mindfulness-Based Stress Reduction (MBSR) A description of social cognition tasks (empathy, theory program (short term meditators, STM) and controls of mind and emotion recognition) is provided in Table 1 (nonmeditators). We predicted that long term practi- (see also Additional file 1: Table S1 for a detailed explan- tioners would show enhanced interoceptive sensitivity, ation of the materials and methods). reflected in a better performance in heartbeat detection and related domains of social cognition. Interoception Methods Heartbeat detection task (HBD) Subjects The HBD is a motor tracking test that assesses intero- Ten nonmeditators, 9 short-term meditators and 10 ception sensitivity [12]. Participants had to tap a key on long-term practitioners participated. The LTP group’s a keyboard along with their heartbeat in different condi- mean was 4.35 (SD = 2.17) years of continued practice tions (see Table 1 and the Additional file 1: Table S1 data and the STM completed an 8-week Mindfulness-Based for a more detailed explanation). Stress Reduction (MBSR) program (see criteria in the Additional file 1: Table S1). Controls had never attended a yoga or meditation course. Groups were age, gender Data analysis and education matched. We controlled body mass index Demographic, neuropsychological, and experimental because it influences the interoceptive performance [18]. data were compared among groups using ANOVA and Participants had no history of drug abuse, neurological Tukey’sHSD post-hoc tests. For categorical variables or psychiatric conditions. Participants provided an (e.g., gender), Kruskal-Wallis tests were applied. Mixed informed consent in accordance with the Declaration of repeated measured ANOVA was performed for HBD, with Helsinki and the study was approved by the institutional a within-subject factor (the four conditions) and a between- ethics committee. subject factor (group). Table 1 Interoception and social cognition domain assessed and tasks employed Interoception Task Description Interoception sensitivity HBD The HBD is a motor tracking test that assesses interoception sensitivity. Participants had to tap a key on a keyboard along with their heartbeat in different conditions. First, as a motor-control condition, participants had to follow an audio-recording of a heartbeat. Next, they had to follow their heartbeat without external feedback (intero-pre condition). Then they had to do the same while receiving simultaneous auditory feedback of their own heart provided through online EKG register (feedback condition). Finally, they had to follow their own heartbeat without feedback (intero-post condition). These conditions offer a measure of audio-motoric performance (first condition), and a cardiac interoceptive measure (second and fourth conditions), prior to and after the feedback condition, respectively. During this task we also measured heart rate and heart rate variability to control their possible influence on interoception sensitivity; results showed no differences among groups (see Additional file 2). Social cognition domain Task Description Emotional recognition Emotional morphing This task assesses recognition of six basic emotion expressions and consists of 48 morphing faces randomly presented on a screen (see Additional file 1). Theory of mind ToM This test assesses the emotional inference aspect of the ToM. Consist of 36 pictures of the eye region of a face. Participants chose which of four words best described the person’s thoughts or feelings in each picture. Empathy IRI The IRI is a 28-item self-report questionnaire that separately measures both the cognitive and affective components of empathy. HBD=Heartbeat Detection task; ToM=Theory of Mind; IRI=Index of Interpersonal Reactivity. Melloni et al. Behavioral and Brain Functions 2013, 9:47 Page 3 of 6 http://www.behavioralandbrainfunctions.com/content/9/1/47 Results df = 25.00) revealed higher scores of depressive symp- Demographic and neuropsychological results toms in controls compared to STM (p < 0.05). We did No differences were found in gender [H = 4.90, p = 0.86], not observe between group differences for STAI-State 2 2 age [F (2, 25) = 0.95, p = 0.39, η 0.07], formal education subscale [F (2, 25) = 1.87, p = 0.17, η = 0.13]. However, p p [F (2, 25) = 2.13, p = 0.13, η = 0.14] or body mass index significant differences for STAI-Trait subscale [F (2, 25) = 2 2 [F (2, 21) = 1.47, p = 0.25, η =0.12] among groups. 3.74, p < 0.05, η = 0.23] were observed; post hoc compar- p p Groups showed similar EF performance measured isons (Tukey test, HSD, MS = 69.98; df = 25.00) showed by the IFS [F (2, 25) =1.50, p=0.24, η =0.10]. There controls had significantly higher anxiety scores (p < 0.05) were no differences in the three condition of the Stroop than LTM. task, word [F (2, 23) = 0.20, p = 0.81, η =0.01], color [F (2, 23) = 1.40, p = 0.26, η =0.10] and incongruent Social cognition measures color-word [F (2, 23) = 0.35, p = 0.70, η =0.03]. No Emotion recognition: No differences were observed regard- interference effect was found [F (2, 23) = 1.88, p = 0.17, ing total accuracy [F (2, 25) = 2.49, p = 0.10, η = 0.16]. η =0.14] (See Table 2). However, per category analysis showed significant differ- ences in disgust recognition among groups [F (2, 25) = 4.1, Clinical evaluation p < 0.05, η = 0.24]. A post-hoc comparison (Tukey HSD We observed a significant difference for BDI score test, MS = 0.01; df = 25.00) revealed lower accuracy among groups [F (2, 25) = 4.12, p < 0.05,, η = 0.24]. performance in LTM group (p < 0.05) than controls (see Post-hoc comparisons (Tukey HSD test, MS = 34.97; Figure 1a). Groups did not differ regarding RTs of average Table 2 Demographic, neuropsychological and clinical results F p Controls STM LTM Gender 4.90 (H) .86 2 M : 8 F 4 M : 4 F 7 M : 3 F M= 37.30; M= 41.12; M= 43.80; Age (years) .95 .40 SD= 9.12 SD= 12.15 SD=10.55 (22 – 49) (25 – 55) (29 – 56) M=16.10; M= 16.13; M= 17.90; Formal education (years) 2.13 .13 SD= .74 SD= 1.73 SD= 3.25 (15 – 17) (12 – 17) (12 – 25) M= 22.94; M= 22.88; M= 24.87; Body mass index 1.47 .25 SD= 2.75 SD= 3.15 SD= 2.49 (19.43 – 26.67) (17.63 – 26.51) (21.60 – 28.57) M= 25.95; M= 27.44; M= 26.25; IFS (Ineco Frontal Score) 1.50 .24 SD= 1.50 SD= 2.47 SD= 1.69 (23 – 28) (23 – 30) (24 – 30) M= 5.02; M= 11.33; M=5.36; Stroop Interference score 1.88 .17 SD= 8.06 SD= 7.20 SD= 7.03 (-6.59 – 15.95) (5.54 – 27.70) (-2.64 – 15.85) M=9.90; M=2.88; M=3.50; BDI-II 4.12 .03 SD=6.94 SD=2.30 SD=6.70 (2 – 22) (0 – 7) (0 – 22) M=40.30; M=33.25; M=30.30; STAI Trait 3.74 .03 SD=9.75 SD=6.54 SD=8.12 (25 – 61) (27 – 43) (23 – 51) M=34.20; M=30.88; M=27.90; STAI State 1.87 .17 SD=10.87 SD=2.70 SD=4.86 (20 – 54) (28 – 34) (23 – 37) M= mean. SD= standard deviation. Numbers within () are min-max. Melloni et al. Behavioral and Brain Functions 2013, 9:47 Page 4 of 6 http://www.behavioralandbrainfunctions.com/content/9/1/47 Figure 1 Social cognition. Emorphing. Percent of accuracy (a) and reaction times in seconds (b) are depicted for every basic emotion and for average scores. Interpersonal reactivity index (IRI). Raw scores of each subscales are presented (c). Reading the mind in the eyes (ToM) Total scores (d). *indicates significant differences. emotions recognition [F (2, 25) = 1.84, p = 0.17, η =0.12]. task that avoids the possible interference of external Conversely, significant differences among groups were stimuli [11] previously reported [5,9]. observed for disgust recognition [F (2, 25) = 3.97, p < 0.05, No differences in EF or demographic variables were η = 0.24]. Post-hoc comparisons showed significantly observed. Related to mood and affective scales, controls slower RT for controls than STM group (p < 0.5). No other showed higher STM (depression) and LTM (anxiety- differences were observed (see Figure 1b). trait) scores. These results might reflect the possible Empathy: Group differences were found in Personal influence of skills acquired during meditation practice distress subscale [F (2, 25) = 7.88, p < 0.01, η =0.38]. (without considering its length), such as stress coping A post-hoc comparison (Tuckey HSD, MS = 13.53; and emotional regulation abilities, which could help to df = 25.00) showed that both LTM and STM groups deal with anxiety and depression situations. These skills scored lower than controls (p < 0.01, for both). No might modulate mood perception as more euthymic and other difference was observed (see Figure 1c). positive [20]. Theory of mind (ToM): No group differences were ob- Regarding interoception, we replicated negative results served [F (2, 25) = 1.10, p = 0.34, η = 0.08] (see Figure 1d). previously reported [5,9]. Body awareness includes one internal (viscera and blood composition) and one exter- nal stream (taste, smell, pressure sensations and pain Interoception [21]). Consequently, cardiac sensations might be consid- No group effects [F (2,25) = 0.57, p = 0.57, η = 0.04] or ered as a basic modality of visceral perception that relies condition × group interaction [F (6, 75) = 0.59, p = 0.72, mostly on internal drive (the heart being an internal η = 0.04] were observed. Thus, there were no signifi- organ), which is why it would be more difficult to gain cant differences in the ability to track their heartbeats conscious inspection. Respiration is unique among (interoceptive conditions) or an external cued heartbeat interoceptive signals as it involves external pressure (motor and feedback conditions), in any of the four information from the nose and chest, and it is suscep- conditions (See Figure 2). Only an expected [12] and ir- tible of voluntary control and straightforward conscious relevant effect of condition was observed (see Additional perception. During meditation, attention is commonly file 2: Table S2). directed towards breathing [5], where more consistent results have been shown [2,7]. These findings suggest Discussion that cardiac perception might not be the most suitable This is the first study assessing the influence of medita- index to reflect meditation influence on interoception. tion practice both in cardiac interoception and in social Few group differences were observed in social cognition cognition using a range of tasks. We selected a HBD domains. The lower accuracy in disgust recognition found Melloni et al. Behavioral and Brain Functions 2013, 9:47 Page 5 of 6 http://www.behavioralandbrainfunctions.com/content/9/1/47 Figure 2 Heartbeat detection task (HBD). The Accuracy Index can vary between 0 and 1, with higher scores indicating better accuracy. No differences were found among groups in any condition. Vertical bars indicate standard deviation. in LTM compared to controls might be related to their was observed. Based on the existence of diverse intero- lower cardiac interoceptive sensitivity (given the common ceptive signals, a more extensive assessment of each insular involvement for interoception and disgust recogni- visceral source (other than cardiac one) may be necessary tion [22]). However, this is speculative because interocep- to disentangle the influence of meditation on interoceptive tive differences were not significant among groups. sensitivity. Both meditators’ groups showed significantly lower em- pathy scores compared to controls only in the personal dis- Additional files tress subscale, an index of emotional contagion by others’ distress [23]. This is unsurprising since one of the aims of Additional file 1: Methods. In this Additional file 1 we provide a supplementary and detailed description of the materials and methods meditation is the regulation of responsiveness to stressors used in the study [24]. Finally, no difference in ToM was observed. Overall, Additional file 2: HBD additional results. In this Additional file 2 we despite the few differences reported, groups have similar provide a supplementary description of others interoceptive results. social cognition performance suggesting that meditation practice in this study may not impact on these abilities. Abbreviations Our study suffers from important limitations. First, the HBD: Heartbeat detection task; LTP: Long term practitioners; STM: Short term meditators; MBSR: Mindfulness-based stress reduction; ToM: Theory of mind; sample size should be increased to allow more informative EF: Executive functions; BDI: Beck’s depression inventory; STAI: State trait analysis (i.e. correlations, multiple regressions) about the anxiety inventory; IFS: INECO frontal screening; IRI: Interpersonal reactivity association among meditation, interoception and social index. cognition. However, it is worth highlighting that we Competing interests reported preliminary data about interoception sensitivity All the authors declare that they have no competing interests with respect measure with a novel method, and that previous research to this study or its publication. has employed similar sample size [9]. Second, further studies should cover a multidimensional interoceptive Authors’ contributions MM and LS collected the data, statistically analyzed the data and wrote the assessment (not only cardiac but also breathing, cardiac, first draft of the manuscript. BC was involved in the study conception and visceral, etc.) and including both awareness and sensibility design, writing the protocol and contributed to the drafting of the dimensions. Finally, groups’ homogeneity should be manuscript. MR contributed in collecting the data and revising the final version of the manuscript. CG contributed to writing the final version of the guaranteed by measuring variables that might bias visceral manuscript. ACJ and MS contributed to revising the final version of the perception such as physical state, volume stroke, blood manuscript. FM contributed to revising the final version of the manuscript. pressure and contractibility (Additional file 2: Table S2). AI is the head of our laboratory, was involved in the study conception and design and contributed to writing the final version of the manuscript. All authors read and approved the final manuscript. Conclusion In conclusion, no influence of meditation practice in Authors’ information cardiac interoception and related social cognition measures Margherita Melloni, Lucas Sedeño as the first author. Melloni et al. Behavioral and Brain Functions 2013, 9:47 Page 6 of 6 http://www.behavioralandbrainfunctions.com/content/9/1/47 Acknowledgements 16. Ahmed FS, Stephen Miller L: Executive function mechanisms of theory of We thank the “Asociación Mindfulness Argentina” for providing the mind. J Autism and Developmental Disorders 2011, 41:667–678. experimental subjects and the place for examination made on this work. 17. Singer T, Lamm C: The social neuroscience of empathy. Ann N Y Acad Sci Specifically, we are grateful for Mrs Clara Badino and Mr Julio Laurindo 2009, 1156:81–96. predisposition to participate and advice on meditator’s sample selection. We 18. Rouse CH, Jones GE, Jones KR: The effect of body composition and also thank all participants of this study. This research was partially supported gender on cardiac awareness. Psychophysiology 1988, 25:400–407. by CONICET, INECO Foundation, CONICYT/FONDECYT Regular (1130920), 19. Torralva T, Roca M, Gleichgerrcht E, Lopez P, Manes F: INECO Frontal FONCyT- PICT 2012–0412, FONCyT- PICT 2012–1309, and James Screening (IFS): a brief, sensitive, and specific tool to assess executive McDonnell Foundation Grants. Any opinions, findings, and conclusions or functions in dementia. J The International Neuropsychological Society: JINS recommendations expressed in this material are those of the authors and 2009, 15:777–786. do not necessarily reflect the views of those grants. 20. 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Davis M: Measuring individual differences in empathy: evidence for a Neuroscience, FCEyN UBA and IFIBA, Conicet, Pabellón 1, Ciudad multidimensional approach. J Personality and Social Psychology 1983, Universitaria, 1428 Buenos Aires, Argentina. National Scientific and Technical 44:113–126. Research Council (CONICET), Buenos Aires, Argentina. Universidad Torcuato 24. Kabat-Zinn J, Nhat Hanh T: Full Catastrophe Living: Using the Wisdom of Your Di Tella, Almirante Juan Saenz Valiente 1010, Buenos Aires, C1428BIJ, Body and Mind to Face Stress, Pain, and Illness. New York: Bantam Dell; 1990. Argentina. Australian Research Council (ACR) Centre of Excellence in Cognition and its Disorders, New South Wales, Australia. doi:10.1186/1744-9081-9-47 Cite this article as: Melloni et al.: Preliminary evidence about the effects Received: 2 August 2013 Accepted: 17 December 2013 of meditation on interoceptive sensitivity and social cognition. Behavioral and Brain Functions 2013 9:47. 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Behavioral and Brain Functions – Springer Journals
Published: Dec 23, 2013