European Journal of Neuroscience, Vol. 13, pp.

16491652, 2001

Federation of European Neuroscience Societies

SHORT COMMUNICATION Neural correlates of religious experience

Nina P. Azari,1,2 Janpeter Nickel,1 Gilbert Wunderlich,1,3 Michael Niedeggen,4 Harald Hefter,1 Lutz Tellmann,3 Hans Herzog,3 Petra Stoerig,4 Dieter Birnbacher5 and Rudiger J. Seitz1
1 2

Department of Neurology, University Hospital Dusseldorf, Germany The Iliff School of Theology/University of Denver, 2201 S, University Blvd, Denver, Colorado 80210, USA 3 Institute of Medicine, Research Center, D-52407 Julich, Germany 4 Department of Physiological Psychology, Heinrich-Heine-University, D-40225 Dusseldorf, Germany 5 Philosophical Institute, Heinrich-Heine-University, D-40225 Dusseldorf, Germany Keywords: brain, human, neuroimaging, PET, religion

Abstract
The commonsense view of religious experience is that it is a preconceptual, immediate affective event. Work in philosophy and psychology, however, suggest that religious experience is an attributional cognitive phenomenon. Here the neural correlates of a religious experience are investigated using functional neuroimaging. During religious recitation, self-identied religious subjects activated a frontalparietal circuit, composed of the dorsolateral prefrontal, dorsomedial frontal and medial parietal cortex. Prior studies indicate that these areas play a profound role in sustaining reexive evaluation of thought. Thus, religious experience may be a cognitive process which, nonetheless, feels immediate.

Introduction
For more than a century, the nature of religious experience has been a topic of considerable scholarship and debate, yet virtually nothing is known about its biological foundations. The commonsense view of religious experience is that it is a preconceptual, immediate affective event (James, 1902; Schleiermacher, 1958. It should be noted that James in The Principles of Psychology (1890) was reluctant to contrast thought and feeling). Work in the philosophy of mind and psychology of religion have challenged this view, suggesting that religious experience may be a cognitive attributional phenomenon (Proudfoot & Shaver, 1975; Shaver, 1975), constituted not simply by the felt immediacy, but by a causal claim regarding a religious source for the personal experience. Therein resides the authority and `force' of the experience (Proudfoot, 1985), rendering religious experience a unique and persistent personal event. We studied a group of self-identied religious subjects, who attributed their religious experience to a biblical psalm, in order to explore for the rst time using functional neuroimaging the brain areas involved in religious experience. While the view that religious experience is a preconceptual feeling would predict the activation of limbic brain areas engaged by emotion, attribution theory would predict brain areas mediating reasoning to be activated. We show that, during religious recitation, religious subjects activated a frontalparietal circuit composed of the dorsolateral prefrontal, dorsomedial frontal and medial parietal cortex, suggesting that religious experience may be a cognitive process.

Methods
Subjects Twelve right-handed, healthy, native-German-speaking adults participated in this study. All had given informed consent to their participation. Six were self-identied as religious (2F, 4M; age, 31 T 3 years), and six were self-identied as non-religious (2F, 4M; age 26 T 3 years). Values are given as mean T SD throughout. The two groups of subjects were matched on education level (25 years university). The religious subjects were members of a `Free Evangelical Fundamentalist Community' in Germany, all of whom reported having had a documented conversion experience, and interpreted biblical text literally as the word of God. For the conversion experience and, hence, for their personal religious experience, the rst verse of biblical Psalm 23 was essential. The religious subjects were teachers at a private secondary school (run by their same faith community), having been selected for their posts on the basis of rigorous faith-based criteria. In this regard, they were a religiously homogeneous group, having religious experience in a personal reproducible manner which could be standardized for the purpose of this study. The non-religious subjects were students at the University of Dusseldorf, who were studying various subjects in the natural sciences. Interaction with the subjects during all study phases was conducted in German by native German speakers. The religious and non-religious subjects did not differ signicantly on imaginability and verbal traits (Imaginability: religious subjects, 27 T 7; nonreligious subjects, 25 T 7, group differences P > 0.5; Verbal: religious subjects, 27 T 8; non-religious subjects, 26 T 6, group differences P > 0.6) (Paivio & Harshman, 1983; this questionaire was translated into German for the purposes of this study), nor did they differ signicantly on personality or life satisfaction measures (P > 0.1, groups different) (Fahrenberg et al., 1984; Eysenck & Eysenck (1975).

Correspondence: Dr Nina P. Azari, 2The Iliff School of Theology, as above. E-mail: nazari@du.edu Received 12 December 2000, revised 8 February 2001, accepted 13 February 2001

1650 N. P. Azari et al.

TABLE 1. Self-assessment ratings for the target state in religious and non-religious subjects after the PET session Happyread Religious subjects Achieve Sustain Non-religious subjects Achieve Sustain 5.8 T 1.9 6.7 T 1.8 6.8 T 1.3 6.8 T 1.2 Happyrecite 5.7 T 1.4 6.2 T 1.2 8.7 T 0.8* 8.2 T 1.2* Religiousread 6.3 T 1.4 6.7 T 1.9 4.2 T 2.2 4.8 T 2.5 Religiousrecite 8.5 T 0.8* 8.3 T 1.6* 5.3 T 2.6 5.0 T 3.0 Neutralread 8.17 T 2.6* 8.17 T 2.6* 9.0 T 0.6* 8.8 T 1.0*

Values are mean T SD for the target state (scale of 110, max is 10) in religious and non-religious subjects. *P < 0.05, paired t-test, different from other task conditions; P < 0.05, two-tailed, independent t-tests, groups different. Note that only the religious subjects achieved the religious state, and only the non-religious subjects achieved the happy state; both groups achieved the neutral state.

themselves and then sustain for the duration of a given scanning session a unique religious state. PET scanning Positron-emission tomography (PET) imaging was approved by the Ethics Committee of Heinrich-Heine-University Dusseldorf (Application #1301). The PET-regional cerebral blood ow (rCBF) data were acquired as described elsewhere (Herzog et al., 1996; Duncan et al., 2000). For this study we used a 24-ring ECAT EXACT-HR camera (resolution 4 mm in-plane, 9 mm FWHM, slice distance 2.4 mm). The session for each subject included six scans separated by 10 min. For each scan, 555 MBq of 15O butanol were injected into the right brachial vein, ushed with saline. PET scanning began at the moment of the injection and lasted for 60 s. The 40 s of dynamically recorded head uptake were used for calculation of the rCBF data. PET image slices were reconstructed using a Hanning lter to an effective image resolution of 9 mm (FWHM) with a slice distance of 2.425 mm. Image analysis was done using SPM97d (http://www.l.ion.ucl.ac.uk/spm). Subjects were PET-scanned in six conditions, inclusive of `religious' and appropriate control conditions: reading silently or reciting (eyes covered) biblical Psalm 23 (1, `religious-read'; 2, `religiousrecite'); reading silently or reciting (eyes covered) the children's nursery rhyme (3, `happy-read'; 4, `happy-recite'); reading silently the set of instructions (5, `neutral-read'); and while lying quietly (eyes covered) (6, `rest'). In the recite conditions (eyes covered), subjects started the task at injection time. In the read conditions, presentation of the stimuli were on a at-screen monitor; horizontal display extent was 12 degrees. For the 30-s preinjection engagement period of the task, the rst half of the text was displayed on the screen and the subject read the text aloud. At the time of the injection and the start of the scanning, the second half of the text was displayed on the screen and the subject read the text silently. These conditions ensured that the subject was fully engaged in the task by the start of the scan, and that all subjects were engaged in the same stimulus material during a given task condition. Task order was pseudo-randomized (`rest' was always rst, and for the religious and happy conditions, `read' was always before `recite'). The felt-quality of each target state was assessed with the Positive Affect Negative Affect Scale (PANAS) (Watson et al., 1988) before and after each PET scan.

FIG. 1. Signicant activations for the contrast `religious-recite' vs. `rest' in religious subjects, rendered onto canonical T1-weighted image of SPM97d (P < 0.001, uncorrected for multiple comparisons) (see also Table 2). Shown are the left, dorsal and right view of the brain. Scans for each subject were realigned and spatially normalized onto the PET template, and smoothed using an isotropic Gaussian kernel with FWHM set at 20 mm. The SPM grey matter threshold was set to its default value. For task comparisons, an ANCOVA (analysis of covariance) model was tted to the data for each voxel.

Stimuli The texts used for the different tasks conditions were: `religious': the rst verse of biblical Psalm 23 (Die Bibel, 1975); `happy': a wellknown German children's nursery rhyme (Lange & Stephan, 1984); and `neutral': instructions on using a phone card from the Dusseldorf telephone book (Deutsche Telekom, 1996). The texts for all stimuli were matched on length, and the rhyme was specially chosen because it was familiar to all subjects and was not associated with music. All subjects were able to recite from memory both the psalm and rhyme at the time of the PET session. According to their responses in prestudy interviews, the religious subjects regarded the induction of repeated, transient religious states in a single scanning session as antithetical to religious experience (and disrespectful to their faith). Thus, they found it acceptable (and were asked) to induce in

Results
During recitation of this psalm, the religious subjects successfully attained the religious state (Table 1). And, as predicted from previous

2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 13, 16491652

Brain acitivity and religious experience

TABLE 2. Peak activations for `religious-recite' in religious subjects Coordinates Brain region R dorsolateral prefrontal (BA 9) L dorsolateral prefrontal (BA 9) dorsomedial frontal (pre-SMA) (BA 6) R medial parietal (precuneus) (BA 7) L cerebellum x 24 28 7 14 2 y 50 36 10 82 48 z 34 32 68 46 20 Z-scores Vs. `rest' 3.74** 3.62** 3.58** 3.57** 3.31** Vs. non-religious 3.29** 2.74*

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Vs. `happy-recite' 3.78** 3.32** 3.32* 2.99*

The Z-scores are shown for the comparisons `religious-recite' vs. `rest' in religious subjects (vs. `rest'); religious vs. non-religious subjects in `religious-recite' (vs. non-religious); and `religious-recite' in religious subjects vs. `happy-recite' in non-religious subjects, i.e. groupQtask interaction effect, (vs. `happy-recite') at **P < 0.001, *P < 0.01, uncorrected. Coordinates (x, y, z in space of Montreal Neurological Institute (MNI) template) and selection of foci according to conventions of SPM97d. Brain regions (approximate Brodmann areas BAs) estimated from Talairach & Tournoux, 1988), after adjustment as appropriate for differences between MNI and Talairach coordinates (http://www.mrc cbu.cam.ac.uk/imaging/mnispace.html).

studies in psychology of religion, demonstrating that religious attributions are commonly directed toward countering or improving negative or `crisis' situations (Spilka et al., 1992), the religious subjects showed a trend toward decreased negative affect during the religious state [PANAS scores for religious subjects in the `religiousrecite' condition: negative postscan (14.0 T 4.5) < negative prescan (15.8 T 6.1), P < 0.09. No other task condition showed changed PANAS values in these subjects, and the non-religious subjects showed no changes in PANAS values (P > 0.5)]. Note that religious experience must be described from the perspective of the subject (Proudfoot, 1985), because the subject's interpretation thereof is central to (constitutive of) the experience. Moreover, there is no acceptable, subject-independent denition of religion or religious (Sharpe, 1983). Thus, attainment of a target state can be determined solely on the basis of subjective self-assessment. The subject achieved and sustained the target state if and only if the subject reported that this was the case (and not, if the reverse). The PET images showed a specic, signicant, activation of the right dorsolateral prefrontal cortex in the religious subjects during the religious state as compared with non-religious subjects. Also as compared to a happy state and a neutral read condition these areas were observed (Fig. 1, Table 2). During the religious state, the religious subjects showed few additional activations, including the dorsomedial frontal cortex and the right precuneus. These activations involved areas that are engaged in cognitive processes, while limbic areas (including the amygdala and orbitofrontal cortex) activated by emotional stimuli (Morris et al., 1996; Paradiso et al., 1997) did not show rCBF changes. As expected, however, the non-religious subjects showed a specic left amygdala activation during the happy state (x = 20, y = 8, z = 22; P < 0.001). Therefore, our results strongly support the view that religious experience is a cognitive attributional phenomenon.

Discussion
Recent neuropsychological and functional imaging studies suggest that the prefrontal cortex holds representations of knowledge structured in the form of cognitive schemas (Partiot et al., 1995). Cognitive schemas are mental representations containing organized prior knowledge about specic domains, inclusive of specications of the causal relations among the attributes therein (Taylor & Crocker, 1981). Religious attributions are made in accordance with religious schemas, which consist in organized knowledge about religion and religious issues, and include reinforced structures for inferring religiously related causality of experienced events (Spilka &

McIntosh, 1995). Prefrontally localized schemas manage such memories stored as representations in posterior brain areas (Grafman & Hendler, 1991), and the dorsolateral prefrontal cortex is critical for memory retrieval and conscious monitoring of thought (Fletcher et al., 1998; McIntosh et al., 1999; Duncan et al., 2000; Gallagher et al., 2000). The medial parietal area activated in the religious subjects was the precuneus, which has strong anatomical connections to prefrontal cortex (Goldman-Rakic, 1988; Petrides & Pandya, 1984), and plays a key role in visual memory (Fletcher et al., 1995). The dorsomedial frontal area we observed corresponds to the presupplementary motor area (pre-SMA) (Rizzolatti et al., 1998). Pre-SMA receives strong inputs from the prefrontal cortex, as well as from the cerebellum (Luppino et al., 1993), the latter of which now is understood to participate in a wide variety of both cognitive and noncognitive processes (Allen et al., 1997). Converging evidence from both animal and human studies indicates that pre-SMA is important in automatically controlling the readiness for action processed by lateral parieto-frontal circuits (Deiber et al., 1991; Tanji et al., 1996), and sustaining the preparation to act based upon the current contents of working memory (Jahanshahi et al., 1995; Haxby et al., 2000). Thus, we suggest that religious experience may be a cognitive process, mediated by a pre-established neural circuit, involving dorsolateral prefrontal, dorsomedial frontal and medial parietal cortex. Because religious attributions are made in anomalous or ambiguous situations, when a person does not know what to expect or what to do, yet actively and persistently seeks a solution, a persistent, internally generated `readiness' emerges, which subsequently serves to re-activate the religious schema in the presence of salient religious cues (Proudfoot, 1985). For the religious subjects of this study, biblical Psalm 23 was the salient religious cue. There is substantial evidence from the psychology of religion to suggest that people are `prepared' for religious experiences (Spilka et al., 1996). This `readiness' is probably mediated by the dorsomedial frontal cortex, leading to the commonly reported felt immediacy of religious experience. The experience, however, becomes religious when the subject has consciously identied it as consistent with the subject's own religious schema (Proudfoot, 1985). This cognitive process most probably involves the dorsolateral prefrontal and medial parietal cortex (Fletcher et al., 1995; Partiot et al., 1995). Consequently, subsequent self-initiated religious actions will reinforce the subject's personal religious schema (Proudfoot, 1985; Spilka & McIntosh, 1995). Notably, the religious experience studied here did not involve activation of limbic areas, although the religious subjects were

2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 13, 16491652

1652 N. P. Azari et al. positively affected by the recital of Psalm 23. Thus, the religious experience was not an emotional experience, nor an arousal comparable to that of the happy state which we observed in the non-religious subjects. Admittedly we used highly standardized stimuli to identify a neurobiological correlate of the concept of `religious experience' in this initial study. A challenge for future work will be to explore transient religious states and the evolution of other varieties of religious experience. It may turn out that `religious experience' can be divided eventually into a variety of subprocesses, as has been, for example, the case with memory.
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Acknowledgements
Supported by grants to N.P. Azari from the Alexander von Humboldt Foundation and the Deutscher Akademischer Austausch Dienst (DAAD), and SFB 194 of the Deutsche Forschungsgemeinschaft to R.J.S. and H.H.

Abbreviations
PANAS, Positive Affect Negative Affect Scale; PET, positron emission tomography; pre-SMA, presupplementary motor area; rCBF, regional cerebral blood ow.

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2001 Federation of European Neuroscience Societies, European Journal of Neuroscience, 13, 16491652