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Effects of long-term meditation practice on attentional biases towards emotional faces: An eye-tracking study a
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S. V. Pavlov , V. V. Korenyok , N. V. Reva , A. V. Tumyalis , K. V. Loktev & L. I. Aftanas
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Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Novosibirsk, Russia Published online: 11 Aug 2014.
Click for updates To cite this article: S. V. Pavlov, V. V. Korenyok, N. V. Reva, A. V. Tumyalis, K. V. Loktev & L. I. Aftanas (2014): Effects of long-term meditation practice on attentional biases towards emotional faces: An eyetracking study, Cognition and Emotion, DOI: 10.1080/02699931.2014.945903 To link to this article: http://dx.doi.org/10.1080/02699931.2014.945903
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COGNITION AND EMOTION, 2014 http://dx.doi.org/10.1080/02699931.2014.945903
Effects of long-term meditation practice on attentional biases towards emotional faces: An eye-tracking study
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S. V. Pavlov, V. V. Korenyok, N. V. Reva, A. V. Tumyalis, K. V. Loktev, and L. I. Aftanas Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Novosibirsk, Russia
Attentional biases towards affective stimuli reflect an individual balance of appetitive and aversive motivational systems. Vigilance in relation to threatening information reflects emotional imbalance, associated with affective and somatic problems. It is known that meditation practice significantly improves control of attention, which is considered to be a tool for adaptive emotional regulation. In this regard, the main aim of the present study was to evaluate the influence of meditation on attentional bias towards neutral and emotional facial expressions. Eyes were tracked while 21 healthy controls and 23 experienced meditators (all males) viewed displays consisting of four facial expressions (neutral, angry, fearful and happy) for 10 s. Measures of biases in initial orienting and maintenance of attention were assessed. No effects were found for initial orienting biases. Meditators spent significantly less time viewing angry and fearful faces than control subjects. Furthermore, meditators selectively attended to happy faces whereas control subjects showed attentional biases towards both angry and happy faces. In sum we can conclude that long-term meditation practice adaptively affects attentional biases towards motivationally significant stimuli and that these biases reflect positive mood and predominance of appetitive motivation. Keywords: Meditation; Emotion; Faces; Eye tracking; Attentional bias.
Recent years have seen a growing interest in meditation as a tool for alternative therapy of stress-related and psychosomatic diseases (for reviews, see Barnes & Orme-Johnson, 2012; Chen et al., 2012; Hagins, States, Selfe, & Innes, 2013;
Khoury et al., 2013). However, little is known about the mechanisms through which meditation and its constituent practices might produce positive health outcomes. One of the possible mechanisms is selfregulation of attention, which is common to the
Correspondence should be addressed to: Sergei V. Pavlov, Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Timakova str., 4, Novosibirsk 630117, Russia. E-mail: [email protected] We thank the members of the Novosibirsk Sahaja yoga regional organisation Dmitry M. Vatnik and Vladimir A. Soloviev for their assistance in organising the research. We also thank Ivan V. Brack, Tatyana E. Rau and Lisa Marie Baranov for their technical assistance in this project. © 2014 Taylor & Francis
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many meditation methods, which can be classified into two types—mindfulness and concentrative— depending on how the attentional processes are mainly directed. However, actually, most meditative techniques lie somewhere on a continuum between these two types (Cahn & Polich, 2006). For example, with regard to mindfulness meditation, recent component-process models propose “attention regulation” as one of the key mechanisms (including also body awareness, emotion regulation and change in perspective on the self) through which mindfulness affects emotion and physiology (Holzel et al., 2011). The role of attention regulation seems to be of primary importance, because it is a necessary component for other mechanisms, especially for different kinds of emotion regulation (Wadlinger & Isaacowitz, 2011). It was found that early phases of mindfulness meditation training, which are more concerned with the development of focused attention, was associated with improvements in selective and executive attention whereas the later phases, which are characterised by an open monitoring of internal and external stimuli, were associated with improvements in orienting and alerting attention and in unfocused sustained attention (Ainsworth, Eddershaw, Meron, Baldwin, & Garner, 2013; Chiesa, Calati, & Serretti, 2011; Holzel et al., 2011). Research on Buddhist contemplative techniques has shown that focused attention meditation improved selective and sustained attention whereas open monitoring meditation was associated with improvements in monitoring, vigilance and disengaging attention from stimuli (Lutz, Slagter, Dunne, & Davidson, 2008). However, despite the fact that meditation improves attention regulation in cognitive tasks, there is a lack of knowledge of the impact of meditation practices on attentional bias towards motivationally significant stimuli. Thus it is well known that anxious individuals show increased vigilance towards threat and difficulty disengaging from threat, whereas depressed individuals are characterised by reduced orienting to positive stimuli, as well as reduced maintenance of gaze on positive stimuli and increased maintenance of gaze on dysphoric stimuli (for reviews, see Armstrong & Olatunji, 2012; BarHaim, Lamy, Pergamin, Bakermans-Kranenburg,
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& van Ijzendoorn, 2007; Cisler & Koster, 2010). If such biases are persistent in healthy individuals, they contribute to the vulnerability to negative information and to the deficits in positive affect and over time may lead to a number of psychiatric, functional somatic and stress-related symptoms (Armstrong & Olatunji, 2012; Williams, Mathews, & MacLeod, 1996). We assume that one of the mechanisms is effective attentional control of the processing of affective stimuli, which prevents maladaptive attentional biases and thereby contributes to positive affectivity. In this regard, there is growing evidence that meditative practices appear to be one of the effective training methodologies in enhancing attentional control (Holzel et al., 2011; Wadlinger & Isaacowitz, 2011). Thus, the objective of this work was to investigate the influence of long-term meditation practice on the information processing of affective stimuli. For this aim we employed an eye-tracking paradigm, because it (1) allows continuous monitoring of the focus of visual orienting, (2) possesses good ecological validity, as people normally look at the stimuli that they attend to and (3) provides measures of biases in initial orienting, as indexed by the direction of the first shift in gaze, as well as in the maintenance of attention, as reflected by the duration of gaze (Caseras, Garner, Bradley, & Mogg, 2007). In order to avoid potential task-related confounds and to evaluate whether there is a default attentional bias in meditators, we investigated shifts of attention while participants performed a passive viewing task. As the stimuli we used emotional faces (angry, fearful and happy), because numerous studies employing different experimental paradigms showed that selective attention to emotional expressions may be a good marker of individual differences in emotional processing and attentional control. Generally it was shown that attentional biases towards threatening faces (angry and fearful) are typical for clinical and non-clinical anxiety (Bar-Haim et al., 2007; Leleu, Douilliez, & Rusinek, 2014), high trait anger individuals (Putman, Hermans, & van Honk, 2004) and severe mood dysregulation (Hommer et al., 2013). In contrast, social phobia and autism are associated
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with an avoidance of facial features, particularly the eyes (Horley, Williams, Gonsalvez, & Gordon, 2004; Tanaka & Sung, 2013). Experimental studies of attentional biases towards happy faces are few and their results are ambiguous. On the one hand, analyses revealed a mood-congruent relation between a positive mood and greater attentional deployment towards happy faces (Sanchez, Vazquez, Gomez, & Joormann, 2014). On the other hand, the results of some studies suggest that attentional bias towards happy faces does not always reflect a positive mood, but often reflect attempts to improve it (Beevers, Ellis, Wells, & McGeary, 2010; Isaacowitz, Toner, Goren, & Wilson, 2008; Koizumi et al., 2013; Sanchez et al., 2014). As a model of meditation, we studied individuals daily practising Sahaja Yoga meditation for more than five years. This technique, largely related to a mindfulness type of meditation, is characterised by a mental state of “thoughtless awareness” or “mental silence” and is accompanied by the experience of bliss. In general, the outcome of this meditative technique, as most others, is a sense of relaxation and positive mood and a feeling of benevolence towards oneself and others (Aftanas & Golocheikine, 2001; Manocha, Black, & Wilson, 2012; Rai, 1993). We realise that case– control type of the present study does not allow to rule out the possibility that pre-meditation cognitive features could be specific of subjects more prone to meditate as compared with control subjects. On the other hand, positive effect of short-term meditation training may be transitory and partially explained by non-specific effects. Therefore, we have focused on long-term effects of meditation, realising the limitations of the design of the present study. The time course of cognitive processing consists of early and late stages (Bar-Haim et al., 2007; Posner & Petersen, 1990). The early (mostly automatic) stage includes stimulus encoding and is accompanied by an involuntary shift of attention towards a motivationally relevant stimulus. The late stage involves mostly voluntary attentional control, guided by expectations and motives, and is associated with “engage” and “disengage” mechanisms,
which hold and release attention between shifts. We assume that the long-term effects of meditation will mainly become apparent at the late stage of stimulus processing, since meditation practice primarily develops voluntary attention, including internalisation of attention, directing sustained attention on a specific object and disengaging attention from distracting stimuli (Wadlinger & Isaacowitz, 2011). In summary, we assume that the meditators compared with control subjects will spend less time viewing angry and fearful faces. Furthermore, we suppose that meditators will maintain their gaze longer on happy faces than on other facial expressions.
METHODS Participants Two groups of healthy right-handed males with normal or corrected-to-normal vision participated in our study. The experimental group included 23 experienced long-term Sahaja Yoga meditators (meditators, M = 36.3, SD = 8.8; mean meditation experience = 12.3 years, SD = 4.53) and 21 agematched healthy controls with no meditation experience (controls, M = 32.8, SD = 6.0). The differences between meditators and controls in age were insignificant (t(42) = −1.54, p > .12). All the subjects gave written informed consent and were paid for participation.
Stimuli Composite images were used as stimuli. Each target image consisted of four faces of the same person (neutral, angry, fearful and happy), including 11 male models [five from Ekman and Friesen’s Pictures of Facial Affect and six from the MacBrain Face Stimulus Set (see http:/www.macbrain.org)]. Faces were cropped into ovals (size: 9° high × 6° wide, distances from nose to nose: 11° × 11° of visual angle), the background was grey and a black fixation cross was placed in the centre of the image. An additional set of images with similar design, but including only neutral faces, was also generated. These erasing images were used in COGNITION AND EMOTION, 2014
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order to cancel the possible effect of previous attentional bias for any facial locations and were not included in the analysis.
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Procedure Subjects were seated in an adjustable chair and the light in the room was dimmed. Participants were asked to view a series of images depicting people’s faces and to “look at the images as they normally would”. Each subject performed a series of 22 trials, each of 11 face models was repeated twice. Each trial began with a blank screen of 2–3 s duration, followed by a fixation cross which appeared at the centre of the screen. Participants had to maintain fixation on the fixation cross for a minimum of 2 s in order to begin the target image, which was presented for 10 s and, followed by an erasing image for 4 s, including the same face model (Figure 1). The arrangement of four facial expressions was counterbalanced across trials. The target images with the same face model could not be presented successively.
Eye-tracking system Line of visual gaze was assessed using a remote optics SMI RED 250 eye-tracking device (SensoMotoric Instruments GmbH, the Netherlands). A 17″ monitor was placed approximately 70 cm before the subject’s eyes. Before the experimental session the tracker was calibrated individually for each participant using a 5-point calibration method integrated in the software. According to this procedure the tracker adjusts and recalibrates until the tracking error values reach 0.5° of the visual angle (for both x and y axis) or lesser. During experimental trials the tracking device
Figure 1. Schematic depiction of the timing of a trial.
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continuously stored coordinates of gaze position on the screen with the frequency of 250 Hz. Eye movement data with a loss of signal due to blinking or off-screen gazes were excluded automatically. Eye movements that were stable for more than 50 ms (minimum fixation duration) within 1° of the visual angle were classified as fixation. Areas of interest were also identified for each trial and corresponded with the total area for each of the four facial expressions cropped into ovals.
Eye-tracking outcomes In order to estimate whether analysed groups differentially attended to a facial expression category, we obtained eye tracking parameters corresponding to initial orienting and maintenance of attention. Initial orienting was assessed by the location of the first fixation (i.e., percentage of the first fixations on a certain facial category in relation to all first fixations on facial expressions). Parameters related to the maintenance of attention were as follows: dwell time (sum of all fixations and saccades), fixation count and fixation time (sum of fixation durations).
Data analysis Group differences were analysed for each eyetracking measure using repeated-measures analysis of variances with the factor of Group (2: controls, meditators) as a between-subject factor and Facial Expression (4: Neutral, Fear, Anger, Happy) as a within-subject factor. For all analyses, the degrees of freedom were Greenhouse–Geisser corrected where appropriate. All post hoc comparisons were
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evaluated by means of the Tukey test. Effect sizes are reported using the partial eta square (g2p ).
RESULTS Initial orienting
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No main effect of group or its interaction with facial expression was found for the location of the first fixation.
Maintenance of attention For dwell time, significant Group × Facial Expression (F(3, 126) = 4.13, p = .024, g2 ¼ .089) interaction was revealed (see Figure 2). Analysis of this interaction showed that meditators in comparison to controls spent less time viewing angry (p < .001) and fearful faces (p = .004). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.40, p = .001, g2 ¼ .299) and controls (F(3, 60) = 8.69, p = .002, g2 ¼ .303), showing that meditators spent more time viewing happy faces as compared to other faces (all p < .022), whereas controls spent more time viewing happy and angry faces as compared to neutral faces (all p < .02) and less time viewing fearful faces in comparison to happy ones (p < .008). For fixation time, significant Group × Facial Expression (F(3, 126) = 4.18, p = .022, g2 ¼ .091) interaction was revealed (see Figure 2). Analysis of this interaction showed that meditators in comparison to controls spent less time viewing angry (p < .001) and fearful faces (p = .010). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.34, p = .001, g2 ¼ .298) and controls (F(3, 60) = 8.60, p = .002, g2 ¼ .301), showing that meditators spent more time viewing happy faces as compared to other faces (all p < .026), whereas controls spent more time viewing happy and angry faces as compared to neutral faces (all p < .020) and less time viewing fearful faces in comparison to happy ones (p < .007). For fixation count, significant Group × Facial Expression (F(3, 126) = 4.35, p = .020, g2 ¼ .094) interaction was revealed (see Figure 2). Analysis of
Figure 2. Means of dwell time, fixation time and fixation count viewing neutral, happy, angry and fearful faces presented by longterm meditation and control groups. Error bars are the standard errors. *Significant between-group differences at p < .05.
this interaction showed that meditators in comparison to controls showed less number of fixations for angry (p < .001) and fearful faces (p = .005). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.24, p = .001, g2 ¼ .296) and controls (F(3, 60) = 7.24, p = .003, g2 ¼ .266), showing that meditators were characterised by greater number of fixations for happy faces as compared to other faces (all p < .019), whereas controls showed greater number of fixations for happy and angry faces as compared to neutral ones (all p < .027). COGNITION AND EMOTION, 2014
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DISCUSSION We tracked eye movements while experienced meditators and control subjects passively viewed displays consisting of three emotional (fearful, angry and happy) faces and one neutral face. We have not revealed evidence for the influence of long-term practice of meditation on the initial orienting to facial expressions, whereas the analysis of maintenance of attention confirmed our hypothesis. Namely, meditators spent significantly less time viewing angry and fearful faces than control subjects and selectively attended to happy faces. It is notable that control subjects showed attentional biases to both angry and happy faces. The latter finding supports the emotionality hypothesis (Lang, Bradley, & Cuthbert, 1997), rather than any form of specificity (e.g., a bias to threatening stimuli), according to which our cognitive system must be motivationally biased to allocate preferential attention to emotional stimuli, irrespective of their valence, due to their special adaptive importance for preservative or protective functions. Other eye-tracking research confirmed this statement, showing that overt visual attention is captured by both unpleasant and pleasant pictures (Nummenmaa, Hyönä, & Calvo, 2006). However, the results of the present study indicate that the findings of the emotionality hypothesis are not applicable to meditators, who demonstrated selective attention only towards happy faces. Recent research has shown that selective attention towards positive stimuli is typical for individuals, who experience higher daily positive mood states (Tamir & Robinson, 2007). If we take into account that Sahaja Yoga meditation practice promotes a positive mood and a feeling of benevolence towards oneself and others, then the revealed effects are consistent with Tamir and Robinson’s findings. Prevalence of positive emotions, in turn, has been shown to broaden individuals’ attention and increase its plasticity, which is crucial for successful emotion regulation (Fredrickson, 1998; Fredrickson, Mancuso, Branigan, & Tugade, 2000). Our results confirm this mechanism, showing that meditators, in contrast to
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the control subjects, did not show a shift of attention towards angry relative to neutral facial expressions. Absence of an attentional bias towards angry faces may reflect a regulatory mechanism, allowing meditators to adaptively take in a minimal amount of information needed from a threatening stimulus to decode its meaning, rather than fixating on its negative details, thus increasing negative affect. Thus, it is likely that the revealed attentional biases in experienced meditators can be considered to be one of the mechanisms of emotional regulation, which helps them to attain and preserve a positive mood (Wadlinger & Isaacowitz, 2008). From the viewpoint of the evaluative space model (Norris, Gollan, Berntson, & Cacioppo, 2010), attentional shift to happy faces in meditators may reflect predominance of positive offset over negativity bias. According to this model, positivity offset results in a tendency to approach and explore novel (but neutral) environments, behaviours that contribute to knowledge about the world around us and, ultimately, to the resources we obtain. As for the possible neurophysiological mechanisms responsible for the differences in attentional biases between meditators and controls, it is necessary to take into account that the early and late stages of cognitive processing of the stimulus provided, respectively, stimulus-driven and goaldirected systems, have various neurophysiological bases (Corbetta & Shulman, 2002; Posner & Petersen, 1990). The stimulus-driven system is specialised for the detection of motivationally relevant stimuli through automatic shifts in attention. The role of the amygdala and temporoparietal cortex is crucial for this system (e.g., LeDoux, 2000; Sander, Grafman, & Zalla, 2003; Vuilleumier, 2005). The goal-directed (top-down, “anterior attentional”) system includes anterior cingulate and superior frontal cortex selects and maintains focus on stimuli according to ongoing plans, resulting in voluntary, “endogenous” shifts of attention as well as the inhibition of exogenous shifts of attention towards distracting stimuli. Observed differences between meditators and controls related only to indicators of maintenance of attention and not to the initial shift of attention, and
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therefore, processes of the goal-directed (top-down) system have been largely influenced by long-term meditation practice. This assumption is partially evidenced by functional magnetic resonance imaging (fMRI) studies indicating increased activation of frontal cortical areas and the anterior cingulate cortex during meditation (for review, see Cahn & Polich, 2006). Moreover, in fMRI research of Desbordes et al. (2012), the longitudinal decrease in right amygdala activation in response to affective images was revealed after training subjects in mindful meditation, which may be explained by increased control of frontal cortical regions. It is important, that with the clear evidence of the impact of meditation practice on the later stages of processing of motivationally relevant stimuli, we did not reveal the effects of meditation on the initial shift of attention. Moreover, we have found no significant effect of facial expression on initial orienting in both meditators and control subjects. Probably, these results can be explained by the moderate emotional intensity of facial expressions, at least insufficient for a differentiated response of evaluative emotional system, including amygdala, manifested in detectable changes in overt attention. This assumption is consistent with a growing body of literature that fails to find a tendency for attention to be initially shifted towards a threat in typical participants (for review, see Bar-Haim et al., 2007). It is likely that the use of stimuli of greater emotional intensity (i.e., affective pictures) could contribute to a clearer manifestation of the effects of facial expression and meditation on the initial orienting.
CONCLUSIONS The results of the study showed the influence of long-term meditation practice on attentional biases towards motivationally significant stimuli. Selective attention towards happy faces and inattention towards negative facial expressions may be considered to be one of the mechanisms of emotional regulation, resulting in positive mood and the prevalence of positive offset over negativity bias.
Manuscript received 13 May Revised manuscript received 2 July Manuscript accepted 15 July First published online 7 August
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REFERENCES Aftanas, L. I., & Golocheikine, S. A. (2001). Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: High-resolution EEG investigation of meditation. Neuroscience Letters, 310(1), 57–60. doi:10.1016/S0304-3940(01)02094-8 Ainsworth, B., Eddershaw, R., Meron, D., Baldwin, D. S., & Garner, M. (2013). The effect of focused attention and open monitoring meditation on attention network function in healthy volunteers. Psychiatry Research, 210, 1226–1231. doi:10.1016/j. psychres.2013.09.002 Armstrong, T., & Olatunji, B. O. (2012). Eye tracking of attention in the affective disorders: A metaanalytic review and synthesis. Clinical Psychology Review, 32, 704–723. doi:10.1016/j.cpr.2012.09.004 Bar-Haim, Y., Lamy, D., Pergamin, L., BakermansKranenburg, M. J., & van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–24. doi:10.1037/ 0033-2909.133.1.1 Barnes, V. A., & Orme-Johnson, D. W. (2012). Prevention and treatment of cardiovascular disease in adolescents and adults through the transcendental meditation® program: A research review update. Current Hypertension Reviews, 8, 227–242. doi:10. 2174/157340212803530411 Beevers, C. G., Ellis, A. J., Wells, T. T., & McGeary, J. E. (2010). Serotonin transporter gene promoter region polymorphism and selective processing of emotional images. Biological Psychology, 83, 260– 265. doi:10.1016/j.biopsycho.2009.08.007 Cahn, B. R., & Polich, J. (2006). Meditation states and traits: EEG, ERP, and neuroimaging studies. Psychological Bulletin, 132, 180–211. doi:10.1037/00332909.132.2.180 Caseras, X., Garner, M., Bradley, B. P., & Mogg, K. (2007). Biases in visual orienting to negative and positive scenes in dysphoria: An eye movement study. Journal of Abnormal Psychology, 116, 491– 497. doi:10.1037/0021-843X.116.3.491
COGNITION AND EMOTION, 2014
7
Downloaded by [Fondren Library, Rice University ] at 04:26 27 September 2014
PAVLOV ET AL.
Chen, K. W., Berger, C. C., Manheimer, E., Forde, D., Magidson, J., Dachman, L., & Lejuez, C. W. (2012). Meditative therapies for reducing anxiety: A systematic review and meta-analysis of randomized controlled trials. Depression and Anxiety, 29, 545– 562. doi:10.1002/da.21964 Chiesa, A., Calati, R., & Serretti, A. (2011). Does mindfulness training improve cognitive abilities? A systematic review of neuropsychological findings. Clinical Psychology Review, 31, 449–464. doi:10.1016/j.cpr.2010.11.003 Cisler, J. M., & Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30, 203–216. doi:10.1016/j. cpr.2009.11.003 Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215. Desbordes, G., Negi, L. T., Pace, T. W. W., Wallace, B. A., Raison, C. L., & Schwartz, E. L. (2012). Effects of mindful-attention and compassion meditation training on amygdala response to emotional stimuli in an ordinary, non-meditative state. Frontiers in Human Neuroscience, 6, 292. doi:10.3389/fnhum. 2012.00292 Fredrickson, B. L. (1998). What good are positive emotions?Review of General Psychology, 2, 300–319. doi:10.1037/1089-2680.2.3.300 Fredrickson, B. L., Mancuso, R. A., Branigan, C., & Tugade, M. M. (2000). The undoing effect of positive emotions. Motivation and Emotion, 24, 237–258. doi:10.1023/A:1010796329158 Hagins, M., States, R., Selfe, T., & Innes, K. (2013). Effectiveness of yoga for hypertension: Systematic review and meta-analysis. Evidence-based Complementary and Alternative Medicine, 2013, 649836. doi:10.1155/2013/649836 Holzel, B. K., Lazar, S. W., Gard, T., SchumanOlivier, Z., Vago, D. R, & Ott, U. (2011). How does mindfulness meditation work? Proposing mechanisms of action from a conceptual and neural perspective. Perspectives on Psychological Science, 6, 537–559. doi:10.1177/1745691611419671 Hommer, R. E., Meyer, A., Stoddard, J., Connolly, M. E., Mogg, K., Bradley, B. P., … Brotman, M. A. (2013). Attention bias to threat faces in severe mood dysregulation. Depression and Anxiety, 31(7), 559– 565. doi:10.1002/da.22145 Horley, K., Williams, L. M., Gonsalvez, C., & Gordon, E. (2004). Face to face: Visual scanpath evidence for
8
COGNITION AND EMOTION, 2014
abnormal processing of facial expressions in social phobia. Psychiatry Research, 127(1–2), 43–53. doi:10.1016/j.psychres.2004.02.016 Isaacowitz, D. M., Toner, K., Goren, D., & Wilson, H. R. (2008). Looking while unhappy: Mood-congruent gaze in young adults, positive gaze in older adults. Psychological Science, 19, 848–853. doi:10.1111/ j.1467-9280.2008.02167.x Khoury, B., Lecomte, T., Fortin, G., Masse, M., Therien, P., Bouchard, V., … Hofmann, S. G. (2013). Mindfulness-based therapy: A comprehensive meta-analysis. Clinical Psychology Review, 33, 763–771. doi:10.1016/j.cpr.2013.05.005 Koizumi, A., Kitagawa, N., Kondo, H. M., Kitamura, M. S., Sato, T., & Kashino, M. (2013). Serotonin transporter gene-linked polymorphism affects detection of facial expressions. PLoS One, 8, e59074. doi:10.1371/journal.pone.0059074 Lang, P. J., Bradley, M. M., & Cuthbert, B. (1997). Motivated attention: Affect, activation, and action. In P. J. Lang, R. F. Simmons, & M. T. Balaban (Eds.) , Attention and orienting: Sensory and motivational processes (pp. 97–135). Mahwah, NJ: Erlbaum. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. doi:10.1146/annurev.neuro.23.1.155 Leleu, V., Douilliez, C., & Rusinek, S. (2014). Difficulty in disengaging attention from threatening facial expressions in anxiety: A new approach in terms of benefits. Journal of Behavior Therapy and Experimental Psychiatry, 45, 203–207. doi:10.1016/j. jbtep.2013.10.007 Lutz, A., Slagter, H. A., Dunne, J. D., & Davidson, R. J. (2008). Attention regulation and monitoring in meditation. Trends in Cognitive Sciences, 12, 163– 169. doi:10.1016/j.tics.2008.01.005 Manocha, R., Black, D., & Wilson, L. (2012). Quality of life and functional health status of long-term meditators. Evidence-based Complementary and Alternative Medicine, 2012, 350674. doi:10.1155/ 2012/350674 Norris, C. J., Gollan, J., Berntson, G. G., & Cacioppo, J. T. (2010). The current status of research on the structure of evaluative space. Biological Psychology, 84, 422–436. doi:10.1016/j.biopsycho.2010.03.011 Nummenmaa, L., Hyönä, J., & Calvo, M. G. (2006). Eye movement assessment of selective attentional capture by emotional pictures. Emotion, 6, 257–268. doi:10.1037/1528-3542.6.2.257 Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of
Downloaded by [Fondren Library, Rice University ] at 04:26 27 September 2014
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Neuroscience, 13(1), 25–42. doi:10.1146/annurev. ne.13.030190.000325 Putman, P., Hermans, E., & van Honk, J. (2004). Emotional stroop performance for masked angry faces: It’s BAS, not BIS. Emotion, 4, 305–311. doi:10.1037/1528-3542.4.3.305 Rai, U. C. (1993). Medical science enlightened. London and New York, NY: Life Eternal Trust. Sanchez, U. C., Vazquez, C., Gomez, D., & Joormann, J. (2014). Gaze-fixation to happy faces predicts mood repair after a negative mood induction. Emotion, 14, 85–94. doi:10.1037/a0034500 Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316. doi:10.1515/REVNEURO.2003.14.4.303 Tamir, M., & Robinson, M. D. (2007). The happy spotlight: Positive mood and selective attention to rewarding information. Personality and Social Psychology Bulletin, 33, 1124–1136. doi:10.1177/0146167207301030
Tanaka, J. W., & Sung, A. (2013). The “Eye Avoidance” Hypothesis of Autism Face Processing. Journal of Autism and Developmental Disorders (Epub ahead of print). PMID: 24150885. Vuilleumier, P. (2005). How brains beware: Neural mechanisms of emotional attention. Trends in Cognitive Sciences, 9, 585–594. doi:10.1016/j.tics.2005. 10.011 Wadlinger, H. A., & Isaacowitz, D. M. (2008). Looking happy: The experimental manipulation of a positive visual attention bias. Emotion, 8, 121–126. doi:10.1037/1528-3542.8.1.121 Wadlinger, H. A., & Isaacowitz, D. M. (2011). Fixing our focus: Training attention to regulate emotion. Personality and Social Psychology Review, 15, 75–102. doi:10.1177/1088868310365565 Williams, J. M. G., Mathews, A., & MacLeod, C. (1996). The emotional stroop task and psychopathology. Psychological Bulletin, 120(1), 3–24. doi:10.103 7/0033-2909.120.1.3
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Cognition and Emotion Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/pcem20
Effects of long-term meditation practice on attentional biases towards emotional faces: An eye-tracking study a
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S. V. Pavlov , V. V. Korenyok , N. V. Reva , A. V. Tumyalis , K. V. Loktev & L. I. Aftanas
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Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Novosibirsk, Russia Published online: 11 Aug 2014.
Click for updates To cite this article: S. V. Pavlov, V. V. Korenyok, N. V. Reva, A. V. Tumyalis, K. V. Loktev & L. I. Aftanas (2014): Effects of long-term meditation practice on attentional biases towards emotional faces: An eyetracking study, Cognition and Emotion, DOI: 10.1080/02699931.2014.945903 To link to this article: http://dx.doi.org/10.1080/02699931.2014.945903
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COGNITION AND EMOTION, 2014 http://dx.doi.org/10.1080/02699931.2014.945903
Effects of long-term meditation practice on attentional biases towards emotional faces: An eye-tracking study
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S. V. Pavlov, V. V. Korenyok, N. V. Reva, A. V. Tumyalis, K. V. Loktev, and L. I. Aftanas Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Novosibirsk, Russia
Attentional biases towards affective stimuli reflect an individual balance of appetitive and aversive motivational systems. Vigilance in relation to threatening information reflects emotional imbalance, associated with affective and somatic problems. It is known that meditation practice significantly improves control of attention, which is considered to be a tool for adaptive emotional regulation. In this regard, the main aim of the present study was to evaluate the influence of meditation on attentional bias towards neutral and emotional facial expressions. Eyes were tracked while 21 healthy controls and 23 experienced meditators (all males) viewed displays consisting of four facial expressions (neutral, angry, fearful and happy) for 10 s. Measures of biases in initial orienting and maintenance of attention were assessed. No effects were found for initial orienting biases. Meditators spent significantly less time viewing angry and fearful faces than control subjects. Furthermore, meditators selectively attended to happy faces whereas control subjects showed attentional biases towards both angry and happy faces. In sum we can conclude that long-term meditation practice adaptively affects attentional biases towards motivationally significant stimuli and that these biases reflect positive mood and predominance of appetitive motivation. Keywords: Meditation; Emotion; Faces; Eye tracking; Attentional bias.
Recent years have seen a growing interest in meditation as a tool for alternative therapy of stress-related and psychosomatic diseases (for reviews, see Barnes & Orme-Johnson, 2012; Chen et al., 2012; Hagins, States, Selfe, & Innes, 2013;
Khoury et al., 2013). However, little is known about the mechanisms through which meditation and its constituent practices might produce positive health outcomes. One of the possible mechanisms is selfregulation of attention, which is common to the
Correspondence should be addressed to: Sergei V. Pavlov, Psychophysiology Laboratory, Federal State Budgetary Institution “Scientific Research Institute of Physiology and Basic Medicine”, Siberian Branch of the Russian Academy of Medical Sciences, Timakova str., 4, Novosibirsk 630117, Russia. E-mail: [email protected] We thank the members of the Novosibirsk Sahaja yoga regional organisation Dmitry M. Vatnik and Vladimir A. Soloviev for their assistance in organising the research. We also thank Ivan V. Brack, Tatyana E. Rau and Lisa Marie Baranov for their technical assistance in this project. © 2014 Taylor & Francis
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many meditation methods, which can be classified into two types—mindfulness and concentrative— depending on how the attentional processes are mainly directed. However, actually, most meditative techniques lie somewhere on a continuum between these two types (Cahn & Polich, 2006). For example, with regard to mindfulness meditation, recent component-process models propose “attention regulation” as one of the key mechanisms (including also body awareness, emotion regulation and change in perspective on the self) through which mindfulness affects emotion and physiology (Holzel et al., 2011). The role of attention regulation seems to be of primary importance, because it is a necessary component for other mechanisms, especially for different kinds of emotion regulation (Wadlinger & Isaacowitz, 2011). It was found that early phases of mindfulness meditation training, which are more concerned with the development of focused attention, was associated with improvements in selective and executive attention whereas the later phases, which are characterised by an open monitoring of internal and external stimuli, were associated with improvements in orienting and alerting attention and in unfocused sustained attention (Ainsworth, Eddershaw, Meron, Baldwin, & Garner, 2013; Chiesa, Calati, & Serretti, 2011; Holzel et al., 2011). Research on Buddhist contemplative techniques has shown that focused attention meditation improved selective and sustained attention whereas open monitoring meditation was associated with improvements in monitoring, vigilance and disengaging attention from stimuli (Lutz, Slagter, Dunne, & Davidson, 2008). However, despite the fact that meditation improves attention regulation in cognitive tasks, there is a lack of knowledge of the impact of meditation practices on attentional bias towards motivationally significant stimuli. Thus it is well known that anxious individuals show increased vigilance towards threat and difficulty disengaging from threat, whereas depressed individuals are characterised by reduced orienting to positive stimuli, as well as reduced maintenance of gaze on positive stimuli and increased maintenance of gaze on dysphoric stimuli (for reviews, see Armstrong & Olatunji, 2012; BarHaim, Lamy, Pergamin, Bakermans-Kranenburg,
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& van Ijzendoorn, 2007; Cisler & Koster, 2010). If such biases are persistent in healthy individuals, they contribute to the vulnerability to negative information and to the deficits in positive affect and over time may lead to a number of psychiatric, functional somatic and stress-related symptoms (Armstrong & Olatunji, 2012; Williams, Mathews, & MacLeod, 1996). We assume that one of the mechanisms is effective attentional control of the processing of affective stimuli, which prevents maladaptive attentional biases and thereby contributes to positive affectivity. In this regard, there is growing evidence that meditative practices appear to be one of the effective training methodologies in enhancing attentional control (Holzel et al., 2011; Wadlinger & Isaacowitz, 2011). Thus, the objective of this work was to investigate the influence of long-term meditation practice on the information processing of affective stimuli. For this aim we employed an eye-tracking paradigm, because it (1) allows continuous monitoring of the focus of visual orienting, (2) possesses good ecological validity, as people normally look at the stimuli that they attend to and (3) provides measures of biases in initial orienting, as indexed by the direction of the first shift in gaze, as well as in the maintenance of attention, as reflected by the duration of gaze (Caseras, Garner, Bradley, & Mogg, 2007). In order to avoid potential task-related confounds and to evaluate whether there is a default attentional bias in meditators, we investigated shifts of attention while participants performed a passive viewing task. As the stimuli we used emotional faces (angry, fearful and happy), because numerous studies employing different experimental paradigms showed that selective attention to emotional expressions may be a good marker of individual differences in emotional processing and attentional control. Generally it was shown that attentional biases towards threatening faces (angry and fearful) are typical for clinical and non-clinical anxiety (Bar-Haim et al., 2007; Leleu, Douilliez, & Rusinek, 2014), high trait anger individuals (Putman, Hermans, & van Honk, 2004) and severe mood dysregulation (Hommer et al., 2013). In contrast, social phobia and autism are associated
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with an avoidance of facial features, particularly the eyes (Horley, Williams, Gonsalvez, & Gordon, 2004; Tanaka & Sung, 2013). Experimental studies of attentional biases towards happy faces are few and their results are ambiguous. On the one hand, analyses revealed a mood-congruent relation between a positive mood and greater attentional deployment towards happy faces (Sanchez, Vazquez, Gomez, & Joormann, 2014). On the other hand, the results of some studies suggest that attentional bias towards happy faces does not always reflect a positive mood, but often reflect attempts to improve it (Beevers, Ellis, Wells, & McGeary, 2010; Isaacowitz, Toner, Goren, & Wilson, 2008; Koizumi et al., 2013; Sanchez et al., 2014). As a model of meditation, we studied individuals daily practising Sahaja Yoga meditation for more than five years. This technique, largely related to a mindfulness type of meditation, is characterised by a mental state of “thoughtless awareness” or “mental silence” and is accompanied by the experience of bliss. In general, the outcome of this meditative technique, as most others, is a sense of relaxation and positive mood and a feeling of benevolence towards oneself and others (Aftanas & Golocheikine, 2001; Manocha, Black, & Wilson, 2012; Rai, 1993). We realise that case– control type of the present study does not allow to rule out the possibility that pre-meditation cognitive features could be specific of subjects more prone to meditate as compared with control subjects. On the other hand, positive effect of short-term meditation training may be transitory and partially explained by non-specific effects. Therefore, we have focused on long-term effects of meditation, realising the limitations of the design of the present study. The time course of cognitive processing consists of early and late stages (Bar-Haim et al., 2007; Posner & Petersen, 1990). The early (mostly automatic) stage includes stimulus encoding and is accompanied by an involuntary shift of attention towards a motivationally relevant stimulus. The late stage involves mostly voluntary attentional control, guided by expectations and motives, and is associated with “engage” and “disengage” mechanisms,
which hold and release attention between shifts. We assume that the long-term effects of meditation will mainly become apparent at the late stage of stimulus processing, since meditation practice primarily develops voluntary attention, including internalisation of attention, directing sustained attention on a specific object and disengaging attention from distracting stimuli (Wadlinger & Isaacowitz, 2011). In summary, we assume that the meditators compared with control subjects will spend less time viewing angry and fearful faces. Furthermore, we suppose that meditators will maintain their gaze longer on happy faces than on other facial expressions.
METHODS Participants Two groups of healthy right-handed males with normal or corrected-to-normal vision participated in our study. The experimental group included 23 experienced long-term Sahaja Yoga meditators (meditators, M = 36.3, SD = 8.8; mean meditation experience = 12.3 years, SD = 4.53) and 21 agematched healthy controls with no meditation experience (controls, M = 32.8, SD = 6.0). The differences between meditators and controls in age were insignificant (t(42) = −1.54, p > .12). All the subjects gave written informed consent and were paid for participation.
Stimuli Composite images were used as stimuli. Each target image consisted of four faces of the same person (neutral, angry, fearful and happy), including 11 male models [five from Ekman and Friesen’s Pictures of Facial Affect and six from the MacBrain Face Stimulus Set (see http:/www.macbrain.org)]. Faces were cropped into ovals (size: 9° high × 6° wide, distances from nose to nose: 11° × 11° of visual angle), the background was grey and a black fixation cross was placed in the centre of the image. An additional set of images with similar design, but including only neutral faces, was also generated. These erasing images were used in COGNITION AND EMOTION, 2014
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order to cancel the possible effect of previous attentional bias for any facial locations and were not included in the analysis.
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Procedure Subjects were seated in an adjustable chair and the light in the room was dimmed. Participants were asked to view a series of images depicting people’s faces and to “look at the images as they normally would”. Each subject performed a series of 22 trials, each of 11 face models was repeated twice. Each trial began with a blank screen of 2–3 s duration, followed by a fixation cross which appeared at the centre of the screen. Participants had to maintain fixation on the fixation cross for a minimum of 2 s in order to begin the target image, which was presented for 10 s and, followed by an erasing image for 4 s, including the same face model (Figure 1). The arrangement of four facial expressions was counterbalanced across trials. The target images with the same face model could not be presented successively.
Eye-tracking system Line of visual gaze was assessed using a remote optics SMI RED 250 eye-tracking device (SensoMotoric Instruments GmbH, the Netherlands). A 17″ monitor was placed approximately 70 cm before the subject’s eyes. Before the experimental session the tracker was calibrated individually for each participant using a 5-point calibration method integrated in the software. According to this procedure the tracker adjusts and recalibrates until the tracking error values reach 0.5° of the visual angle (for both x and y axis) or lesser. During experimental trials the tracking device
Figure 1. Schematic depiction of the timing of a trial.
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continuously stored coordinates of gaze position on the screen with the frequency of 250 Hz. Eye movement data with a loss of signal due to blinking or off-screen gazes were excluded automatically. Eye movements that were stable for more than 50 ms (minimum fixation duration) within 1° of the visual angle were classified as fixation. Areas of interest were also identified for each trial and corresponded with the total area for each of the four facial expressions cropped into ovals.
Eye-tracking outcomes In order to estimate whether analysed groups differentially attended to a facial expression category, we obtained eye tracking parameters corresponding to initial orienting and maintenance of attention. Initial orienting was assessed by the location of the first fixation (i.e., percentage of the first fixations on a certain facial category in relation to all first fixations on facial expressions). Parameters related to the maintenance of attention were as follows: dwell time (sum of all fixations and saccades), fixation count and fixation time (sum of fixation durations).
Data analysis Group differences were analysed for each eyetracking measure using repeated-measures analysis of variances with the factor of Group (2: controls, meditators) as a between-subject factor and Facial Expression (4: Neutral, Fear, Anger, Happy) as a within-subject factor. For all analyses, the degrees of freedom were Greenhouse–Geisser corrected where appropriate. All post hoc comparisons were
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evaluated by means of the Tukey test. Effect sizes are reported using the partial eta square (g2p ).
RESULTS Initial orienting
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No main effect of group or its interaction with facial expression was found for the location of the first fixation.
Maintenance of attention For dwell time, significant Group × Facial Expression (F(3, 126) = 4.13, p = .024, g2 ¼ .089) interaction was revealed (see Figure 2). Analysis of this interaction showed that meditators in comparison to controls spent less time viewing angry (p < .001) and fearful faces (p = .004). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.40, p = .001, g2 ¼ .299) and controls (F(3, 60) = 8.69, p = .002, g2 ¼ .303), showing that meditators spent more time viewing happy faces as compared to other faces (all p < .022), whereas controls spent more time viewing happy and angry faces as compared to neutral faces (all p < .02) and less time viewing fearful faces in comparison to happy ones (p < .008). For fixation time, significant Group × Facial Expression (F(3, 126) = 4.18, p = .022, g2 ¼ .091) interaction was revealed (see Figure 2). Analysis of this interaction showed that meditators in comparison to controls spent less time viewing angry (p < .001) and fearful faces (p = .010). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.34, p = .001, g2 ¼ .298) and controls (F(3, 60) = 8.60, p = .002, g2 ¼ .301), showing that meditators spent more time viewing happy faces as compared to other faces (all p < .026), whereas controls spent more time viewing happy and angry faces as compared to neutral faces (all p < .020) and less time viewing fearful faces in comparison to happy ones (p < .007). For fixation count, significant Group × Facial Expression (F(3, 126) = 4.35, p = .020, g2 ¼ .094) interaction was revealed (see Figure 2). Analysis of
Figure 2. Means of dwell time, fixation time and fixation count viewing neutral, happy, angry and fearful faces presented by longterm meditation and control groups. Error bars are the standard errors. *Significant between-group differences at p < .05.
this interaction showed that meditators in comparison to controls showed less number of fixations for angry (p < .001) and fearful faces (p = .005). Additionally, significant effects of facial expression were revealed for meditators (F(3, 66) = 9.24, p = .001, g2 ¼ .296) and controls (F(3, 60) = 7.24, p = .003, g2 ¼ .266), showing that meditators were characterised by greater number of fixations for happy faces as compared to other faces (all p < .019), whereas controls showed greater number of fixations for happy and angry faces as compared to neutral ones (all p < .027). COGNITION AND EMOTION, 2014
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DISCUSSION We tracked eye movements while experienced meditators and control subjects passively viewed displays consisting of three emotional (fearful, angry and happy) faces and one neutral face. We have not revealed evidence for the influence of long-term practice of meditation on the initial orienting to facial expressions, whereas the analysis of maintenance of attention confirmed our hypothesis. Namely, meditators spent significantly less time viewing angry and fearful faces than control subjects and selectively attended to happy faces. It is notable that control subjects showed attentional biases to both angry and happy faces. The latter finding supports the emotionality hypothesis (Lang, Bradley, & Cuthbert, 1997), rather than any form of specificity (e.g., a bias to threatening stimuli), according to which our cognitive system must be motivationally biased to allocate preferential attention to emotional stimuli, irrespective of their valence, due to their special adaptive importance for preservative or protective functions. Other eye-tracking research confirmed this statement, showing that overt visual attention is captured by both unpleasant and pleasant pictures (Nummenmaa, Hyönä, & Calvo, 2006). However, the results of the present study indicate that the findings of the emotionality hypothesis are not applicable to meditators, who demonstrated selective attention only towards happy faces. Recent research has shown that selective attention towards positive stimuli is typical for individuals, who experience higher daily positive mood states (Tamir & Robinson, 2007). If we take into account that Sahaja Yoga meditation practice promotes a positive mood and a feeling of benevolence towards oneself and others, then the revealed effects are consistent with Tamir and Robinson’s findings. Prevalence of positive emotions, in turn, has been shown to broaden individuals’ attention and increase its plasticity, which is crucial for successful emotion regulation (Fredrickson, 1998; Fredrickson, Mancuso, Branigan, & Tugade, 2000). Our results confirm this mechanism, showing that meditators, in contrast to
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the control subjects, did not show a shift of attention towards angry relative to neutral facial expressions. Absence of an attentional bias towards angry faces may reflect a regulatory mechanism, allowing meditators to adaptively take in a minimal amount of information needed from a threatening stimulus to decode its meaning, rather than fixating on its negative details, thus increasing negative affect. Thus, it is likely that the revealed attentional biases in experienced meditators can be considered to be one of the mechanisms of emotional regulation, which helps them to attain and preserve a positive mood (Wadlinger & Isaacowitz, 2008). From the viewpoint of the evaluative space model (Norris, Gollan, Berntson, & Cacioppo, 2010), attentional shift to happy faces in meditators may reflect predominance of positive offset over negativity bias. According to this model, positivity offset results in a tendency to approach and explore novel (but neutral) environments, behaviours that contribute to knowledge about the world around us and, ultimately, to the resources we obtain. As for the possible neurophysiological mechanisms responsible for the differences in attentional biases between meditators and controls, it is necessary to take into account that the early and late stages of cognitive processing of the stimulus provided, respectively, stimulus-driven and goaldirected systems, have various neurophysiological bases (Corbetta & Shulman, 2002; Posner & Petersen, 1990). The stimulus-driven system is specialised for the detection of motivationally relevant stimuli through automatic shifts in attention. The role of the amygdala and temporoparietal cortex is crucial for this system (e.g., LeDoux, 2000; Sander, Grafman, & Zalla, 2003; Vuilleumier, 2005). The goal-directed (top-down, “anterior attentional”) system includes anterior cingulate and superior frontal cortex selects and maintains focus on stimuli according to ongoing plans, resulting in voluntary, “endogenous” shifts of attention as well as the inhibition of exogenous shifts of attention towards distracting stimuli. Observed differences between meditators and controls related only to indicators of maintenance of attention and not to the initial shift of attention, and
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therefore, processes of the goal-directed (top-down) system have been largely influenced by long-term meditation practice. This assumption is partially evidenced by functional magnetic resonance imaging (fMRI) studies indicating increased activation of frontal cortical areas and the anterior cingulate cortex during meditation (for review, see Cahn & Polich, 2006). Moreover, in fMRI research of Desbordes et al. (2012), the longitudinal decrease in right amygdala activation in response to affective images was revealed after training subjects in mindful meditation, which may be explained by increased control of frontal cortical regions. It is important, that with the clear evidence of the impact of meditation practice on the later stages of processing of motivationally relevant stimuli, we did not reveal the effects of meditation on the initial shift of attention. Moreover, we have found no significant effect of facial expression on initial orienting in both meditators and control subjects. Probably, these results can be explained by the moderate emotional intensity of facial expressions, at least insufficient for a differentiated response of evaluative emotional system, including amygdala, manifested in detectable changes in overt attention. This assumption is consistent with a growing body of literature that fails to find a tendency for attention to be initially shifted towards a threat in typical participants (for review, see Bar-Haim et al., 2007). It is likely that the use of stimuli of greater emotional intensity (i.e., affective pictures) could contribute to a clearer manifestation of the effects of facial expression and meditation on the initial orienting.
CONCLUSIONS The results of the study showed the influence of long-term meditation practice on attentional biases towards motivationally significant stimuli. Selective attention towards happy faces and inattention towards negative facial expressions may be considered to be one of the mechanisms of emotional regulation, resulting in positive mood and the prevalence of positive offset over negativity bias.
Manuscript received 13 May Revised manuscript received 2 July Manuscript accepted 15 July First published online 7 August
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REFERENCES Aftanas, L. I., & Golocheikine, S. A. (2001). Human anterior and frontal midline theta and lower alpha reflect emotionally positive state and internalized attention: High-resolution EEG investigation of meditation. Neuroscience Letters, 310(1), 57–60. doi:10.1016/S0304-3940(01)02094-8 Ainsworth, B., Eddershaw, R., Meron, D., Baldwin, D. S., & Garner, M. (2013). The effect of focused attention and open monitoring meditation on attention network function in healthy volunteers. Psychiatry Research, 210, 1226–1231. doi:10.1016/j. psychres.2013.09.002 Armstrong, T., & Olatunji, B. O. (2012). Eye tracking of attention in the affective disorders: A metaanalytic review and synthesis. Clinical Psychology Review, 32, 704–723. doi:10.1016/j.cpr.2012.09.004 Bar-Haim, Y., Lamy, D., Pergamin, L., BakermansKranenburg, M. J., & van Ijzendoorn, M. H. (2007). Threat-related attentional bias in anxious and nonanxious individuals: A meta-analytic study. Psychological Bulletin, 133(1), 1–24. doi:10.1037/ 0033-2909.133.1.1 Barnes, V. A., & Orme-Johnson, D. W. (2012). Prevention and treatment of cardiovascular disease in adolescents and adults through the transcendental meditation® program: A research review update. Current Hypertension Reviews, 8, 227–242. doi:10. 2174/157340212803530411 Beevers, C. G., Ellis, A. J., Wells, T. T., & McGeary, J. E. (2010). Serotonin transporter gene promoter region polymorphism and selective processing of emotional images. Biological Psychology, 83, 260– 265. doi:10.1016/j.biopsycho.2009.08.007 Cahn, B. R., & Polich, J. (2006). Meditation states and traits: EEG, ERP, and neuroimaging studies. Psychological Bulletin, 132, 180–211. doi:10.1037/00332909.132.2.180 Caseras, X., Garner, M., Bradley, B. P., & Mogg, K. (2007). Biases in visual orienting to negative and positive scenes in dysphoria: An eye movement study. Journal of Abnormal Psychology, 116, 491– 497. doi:10.1037/0021-843X.116.3.491
COGNITION AND EMOTION, 2014
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PAVLOV ET AL.
Chen, K. W., Berger, C. C., Manheimer, E., Forde, D., Magidson, J., Dachman, L., & Lejuez, C. W. (2012). Meditative therapies for reducing anxiety: A systematic review and meta-analysis of randomized controlled trials. Depression and Anxiety, 29, 545– 562. doi:10.1002/da.21964 Chiesa, A., Calati, R., & Serretti, A. (2011). Does mindfulness training improve cognitive abilities? A systematic review of neuropsychological findings. Clinical Psychology Review, 31, 449–464. doi:10.1016/j.cpr.2010.11.003 Cisler, J. M., & Koster, E. H. W. (2010). Mechanisms of attentional biases towards threat in anxiety disorders: An integrative review. Clinical Psychology Review, 30, 203–216. doi:10.1016/j. cpr.2009.11.003 Corbetta, M., & Shulman, G. L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nature Reviews Neuroscience, 3(3), 201–215. Desbordes, G., Negi, L. T., Pace, T. W. W., Wallace, B. A., Raison, C. L., & Schwartz, E. L. (2012). Effects of mindful-attention and compassion meditation training on amygdala response to emotional stimuli in an ordinary, non-meditative state. Frontiers in Human Neuroscience, 6, 292. doi:10.3389/fnhum. 2012.00292 Fredrickson, B. L. (1998). What good are positive emotions?Review of General Psychology, 2, 300–319. doi:10.1037/1089-2680.2.3.300 Fredrickson, B. L., Mancuso, R. A., Branigan, C., & Tugade, M. M. (2000). The undoing effect of positive emotions. Motivation and Emotion, 24, 237–258. doi:10.1023/A:1010796329158 Hagins, M., States, R., Selfe, T., & Innes, K. (2013). Effectiveness of yoga for hypertension: Systematic review and meta-analysis. Evidence-based Complementary and Alternative Medicine, 2013, 649836. doi:10.1155/2013/649836 Holzel, B. K., Lazar, S. W., Gard, T., SchumanOlivier, Z., Vago, D. R, & Ott, U. (2011). How does mindfulness meditation work? Proposing mechanisms of action from a conceptual and neural perspective. Perspectives on Psychological Science, 6, 537–559. doi:10.1177/1745691611419671 Hommer, R. E., Meyer, A., Stoddard, J., Connolly, M. E., Mogg, K., Bradley, B. P., … Brotman, M. A. (2013). Attention bias to threat faces in severe mood dysregulation. Depression and Anxiety, 31(7), 559– 565. doi:10.1002/da.22145 Horley, K., Williams, L. M., Gonsalvez, C., & Gordon, E. (2004). Face to face: Visual scanpath evidence for
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abnormal processing of facial expressions in social phobia. Psychiatry Research, 127(1–2), 43–53. doi:10.1016/j.psychres.2004.02.016 Isaacowitz, D. M., Toner, K., Goren, D., & Wilson, H. R. (2008). Looking while unhappy: Mood-congruent gaze in young adults, positive gaze in older adults. Psychological Science, 19, 848–853. doi:10.1111/ j.1467-9280.2008.02167.x Khoury, B., Lecomte, T., Fortin, G., Masse, M., Therien, P., Bouchard, V., … Hofmann, S. G. (2013). Mindfulness-based therapy: A comprehensive meta-analysis. Clinical Psychology Review, 33, 763–771. doi:10.1016/j.cpr.2013.05.005 Koizumi, A., Kitagawa, N., Kondo, H. M., Kitamura, M. S., Sato, T., & Kashino, M. (2013). Serotonin transporter gene-linked polymorphism affects detection of facial expressions. PLoS One, 8, e59074. doi:10.1371/journal.pone.0059074 Lang, P. J., Bradley, M. M., & Cuthbert, B. (1997). Motivated attention: Affect, activation, and action. In P. J. Lang, R. F. Simmons, & M. T. Balaban (Eds.) , Attention and orienting: Sensory and motivational processes (pp. 97–135). Mahwah, NJ: Erlbaum. LeDoux, J. E. (2000). Emotion circuits in the brain. Annual Review of Neuroscience, 23, 155–184. doi:10.1146/annurev.neuro.23.1.155 Leleu, V., Douilliez, C., & Rusinek, S. (2014). Difficulty in disengaging attention from threatening facial expressions in anxiety: A new approach in terms of benefits. Journal of Behavior Therapy and Experimental Psychiatry, 45, 203–207. doi:10.1016/j. jbtep.2013.10.007 Lutz, A., Slagter, H. A., Dunne, J. D., & Davidson, R. J. (2008). Attention regulation and monitoring in meditation. Trends in Cognitive Sciences, 12, 163– 169. doi:10.1016/j.tics.2008.01.005 Manocha, R., Black, D., & Wilson, L. (2012). Quality of life and functional health status of long-term meditators. Evidence-based Complementary and Alternative Medicine, 2012, 350674. doi:10.1155/ 2012/350674 Norris, C. J., Gollan, J., Berntson, G. G., & Cacioppo, J. T. (2010). The current status of research on the structure of evaluative space. Biological Psychology, 84, 422–436. doi:10.1016/j.biopsycho.2010.03.011 Nummenmaa, L., Hyönä, J., & Calvo, M. G. (2006). Eye movement assessment of selective attentional capture by emotional pictures. Emotion, 6, 257–268. doi:10.1037/1528-3542.6.2.257 Posner, M. I., & Petersen, S. E. (1990). The attention system of the human brain. Annual Review of
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ATTENTIONAL BIASES TOWARDS EMOTIONAL FACES
Neuroscience, 13(1), 25–42. doi:10.1146/annurev. ne.13.030190.000325 Putman, P., Hermans, E., & van Honk, J. (2004). Emotional stroop performance for masked angry faces: It’s BAS, not BIS. Emotion, 4, 305–311. doi:10.1037/1528-3542.4.3.305 Rai, U. C. (1993). Medical science enlightened. London and New York, NY: Life Eternal Trust. Sanchez, U. C., Vazquez, C., Gomez, D., & Joormann, J. (2014). Gaze-fixation to happy faces predicts mood repair after a negative mood induction. Emotion, 14, 85–94. doi:10.1037/a0034500 Sander, D., Grafman, J., & Zalla, T. (2003). The human amygdala: An evolved system for relevance detection. Reviews in the Neurosciences, 14, 303–316. doi:10.1515/REVNEURO.2003.14.4.303 Tamir, M., & Robinson, M. D. (2007). The happy spotlight: Positive mood and selective attention to rewarding information. Personality and Social Psychology Bulletin, 33, 1124–1136. doi:10.1177/0146167207301030
Tanaka, J. W., & Sung, A. (2013). The “Eye Avoidance” Hypothesis of Autism Face Processing. Journal of Autism and Developmental Disorders (Epub ahead of print). PMID: 24150885. Vuilleumier, P. (2005). How brains beware: Neural mechanisms of emotional attention. Trends in Cognitive Sciences, 9, 585–594. doi:10.1016/j.tics.2005. 10.011 Wadlinger, H. A., & Isaacowitz, D. M. (2008). Looking happy: The experimental manipulation of a positive visual attention bias. Emotion, 8, 121–126. doi:10.1037/1528-3542.8.1.121 Wadlinger, H. A., & Isaacowitz, D. M. (2011). Fixing our focus: Training attention to regulate emotion. Personality and Social Psychology Review, 15, 75–102. doi:10.1177/1088868310365565 Williams, J. M. G., Mathews, A., & MacLeod, C. (1996). The emotional stroop task and psychopathology. Psychological Bulletin, 120(1), 3–24. doi:10.103 7/0033-2909.120.1.3
COGNITION AND EMOTION, 2014
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