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. Author manuscript; available in PMC: 2020 Oct 15.
Published in final edited form as: Neurosci Lett. 2019 Aug 17;711:134441. doi: 10.1016/j.neulet.2019.134441

A Brief Report: A single case design to examine short-term intracranial EEG patterns during focused meditation

Dana Dharmakaya Colgan 1, Tab Memmott 1, Dan Klee 1, Lia Ernst 1, Seunggu J Han 1, Barry Oken 1
PMCID: PMC6779128  NIHMSID: NIHMS1538256  PMID: 31430545

Abstract

Purpose

This study used a multiple crossover ABAB single case design to examine intracranial EEG data during a breath awareness meditation and an active control task.

Results

Visual analyses suggest that a brief breath awareness mediation was consistently associated with increased alpha power when compared to the active control. Less consistent effects were found with theta, beta, and high gamma activity. Nonparametric t-tests provided additional support for this finding.

Conclusions

Acquiring intracranial EEG patterns during a meditative state may provide more insight into the physiology of meditation with less contamination of high-frequency muscle activity. While access to intracranial EEG during meditation is rarely available, single case design studies are considered adaptations of interrupted time-series designs and can provide an experimental evaluation of intervention effects

Keywords: Meditation, Intracranial EEG, Single Case Experimental Designs, Breath Awareness Meditation

Introduction

Meditation is a type of mental training shown to produce cognitive benefits (Lutz, Slagter, Dunne, & Davidson, 2008). Focused awareness meditation entails voluntarily focusing attention on a chosen object in a sustained fashion. This practice has been shown to enhance attention allocation, emotion regulation, self-awareness, and cognitive control of conflict (Jha et al., 2007). Many studies have employed cross-sectional designs to compare scalp electroencephalography (EEG) activity between experienced meditators and controls (Atchley et al., 2016; Farb et al., 2010; Brefczynski-Lewis, Lutz, Schaefer, Levinson, & Davidson, 2010). Fewer studies have reported on short-term, within-subject EEG differences between meditation and control conditions. The effects of meditation on EEG activity have been investigated by assessing change in oscillatory power of a particular frequency band (Ahani et al., 2013) or oscillatory synchrony, which quantifies change in the degree of phase-locking between different narrow band signals (Lachaux et al., 2010). Increased activity in theta and alpha bands are consistent EEG findings associated with meditation (Lomas et al., 2015). Breath awareness practice, specifically, has been associated with increased alpha (Dunn et al., 1999; Huang & Lo, 2009; Milz et al. 2014; Yu et al., 2011), theta (Huang & Lo, 2009; Takahashi et al., 2005; Tanaka et al., 2014), and beta spectral power (Huang & Lo, 2009). There are also reports of decreased beta (Sagger et al., 2012) and theta (Yu et al., 2011) during breath awareness practice. To add further complications, high-frequency neural activity overlaps with the spectral bandwidth of muscle activity (~20–300 Hz). Therefore, muscle activity may contribute to reports of high-frequency activity recorded with scalp EEG (Muthukumaraswamy, 2013; Whitham et al., 2007).

Acquiring intracranial EEG (iEEG) patterns during a meditative state may provide more insight into the physiology of meditation with less contamination of high-frequency muscle activity. While access to iEEG during meditation is rarely available, single case design studies are considered adaptations of interrupted time-series designs and can provide an experimental evaluation of intervention effects, such as meditation on iEEG (Parsonson et al., 1992; Cook, Campbell, Shadish, 2002). Therefore, the aim of this study was to employ a single case design to analyze iEEG data collected during a breath awareness practice, when compared to an active control activity, in a single person undergoing an awake craniotomy.

Methods

This study used a multiple-crossover ABAB single case design without randomization or blinding. iEEG data were recorded during a breath awareness meditation and an active control task (reminiscing) in the operating room during an awake craniotomy for tumor resection. This case was studied under a broad Institutional Review Board (IRB) protocol of people undergoing brain lesion resection while awake with functional cortical localization. The study was approved by the Oregon Health and Science University’s IRB and the participant provided informed consent prior to assessments.

Participant

The participant was a 32-year old, right-handed, Caucasian male undergoing a resection of a left frontal cortical and juxtacortical low grade astrocytoma adjacent to the precentral gyrus. A week prior to the awake craniotomy, the participant demonstrated no impairments on a cognitive screening that included the Boston Diagnostic Aphasia Examination-Short Form (Goodglass, 2000), Wechsler Adult Intelligence Scale-III Digit Span subtest, Wechsler Memory Scale-III- Logical Memory, and Letter-Number Sequence subtests (Wechsler, 1991). Mental health screening indicated mild depression and moderate anxiety. The participant reported 2200 hours of mindfulness meditation practice over the last five years. The length of training was estimated based on his daily practice and time spent in meditative retreats: The participant attended a 10-day Vipassana retreat and two full-day Mindfulness-Based Stress Reduction retreats. Body scan, open monitoring, and breath awareness were cited as most frequently practiced techniques.

Local anesthetics (lidocaine and marcaine with epinephrine) were administered into planned forehead pin site and for scalp block near head peripheral nerves. The participant was asleep during the craniotomy with dexmedetomidine drip along with briefer course of propofol. These anesthetics were stopped and the participant was awakened for the functional localization of language and this meditation study. At this point, he was able to name all administered pictures from the Boston NamingTest, complete reading and motor tasks, and engage in thoughful conversation. In addition to the anesthetics, the participant was on the anti-seizure medication keppra. During his two-week postoperative appointment, the participant recalled the meditation trial in detail.

Instructions Provided

Instructions were reviewed in the preoperative holding area and in the operating room. Instructions were as follows: “I would like you to close your eyes and remember a travel experience. Allow your mind to roam and remember these experiences with as much detail as you can. After one minute has passed, I will ask you to stop reminiscing and begin a breath awareness meditation. During the meditation, please pay attention the physical sensations of breath wherever you feel it most strongly in the body: Trying not to change the breath, simply cultivating a kind, gentle awareness of the breath moving in and out of the body. Following this short meditation, I will again ask you to ‘Reminisce.’ Like before, please remember a travel experience. Then I will ask you to stop reminiscing and again, begin your breath awareness meditation. During these tasks, please do not speak.”

EEG Recordings and Signal Processing

iEEG was acquired using 4 × 5 subdural electrode strip (Ad-Tech Medical) placed over the left posterior-inferior frontal cortex and recorded and digitized at a sampling rate of 1200 Hz. The CortiQ g.HIamp (Guger Technologies) amplifier used a 24-bit resolution. Each channel had its own synchronized analog to digital converter operating at 614.4 kHz. Grid channels 1 through 18 were referenced to channel 19, which was placed at a distance from locations of eloquent cortex. Data were analyzed offline using BrainVision Analyzer version 2.1. All channels were filtered with a zero-phase shift Butterworth IIR filter. Filter settings included low and high cutoffs of 2 Hz and 240 Hz, respectively, with a 60 Hz notch filter. Data were segmented into 2-second windows using Bartlett’s method. A Fast Fourier Transform with a periodic Hanning window of 20% was used to extract power from each segment in each condition. The FFT band export function was then used to export mean activity per spectral line, measured in power (μV2) for theta (4–8 Hz), alpha (8–13 Hz), beta (13–30 Hz), low gamma (30–50 Hz), and high gamma (70–120 Hz) bands. Outliers, defined as any data point more than 1.5 interquartile ranges below the first quartile or above the third quartile, were removed. Since there were no a priori hypotheses that differentiated the 18 closely spaced cortical electrode locations, and in order to reduce the numbers of dependent variables, the data were reduced by simply averaging across the 18 electrodes at each epoch. A three-point smooth was used to reduce short-term nonstationarities (Tarvainen, Hiltunen, Ranta-aho, & Karjalainen, 2004). Analysis and interpretation was based on prior single-case design studies with multiple crossover (Shadish & Sullivan, 2011; Gabler, Duan, Vohra & Kravitz 2011). We did not evaluate synchrony because the very close proximity of all the cortical electrodes limited the utility of any synchrony measure.

Analyses

Visual analysis of graphic displays of data is a cornerstone of single case experimental designs (Lane & Gast, 2014) and provides evidence for a possible causal relation between the introduction or removal of meditation and change in spectral power. Determining whether or not a brief breath awareness mediation produced dramatic, replicable changes in behavior that last over time was evaluated by examining the level and stability of the data (Cooper et al., 2007). Level is defined as the relative value or magnitude of the data pattern (Wolery & Harris) and was evaluated through the median value of spectral power during each experimental block, for each band. Stability is defined as the variability, or lack of variability, in the data in each experimental block and was calculated by the percent of data points on or within +- 25% of the median (Lane & Gast, 2014). The stability criterion was set to 70% of data points within +- 25% of the median power. Following visual analyses, Friedman tests were conducted on each of the five bands (theta, alpha, beta, low gamma, high gamma) independently. The Friedman test is a nonparametric test used for one-sample, repeated measures designs (with three or more correlated or repeated outcomes) whose distribution is not normal. To identify which pairwise groups demonstrate significant differences, post-hoc analyses were conducted using the Wilcoxon signed rank test with adjusting Bonferroni-corrected alpha level (0.05/3 = 0.0167). The effect size for the Wilcoxon is reported using the r statistic (small effect = .1; medium =.3; large = .5; Field, 2013).

Results

Visual analyses suggested that a brief breath awareness mediation was consistently associated with increased alpha power acquired from iEEG when compared to reminiscing. Results revealed that during the four sequential blocks, alpha power demonstrated consistent level changes following the introduction or removal of meditation. Further, the data appeared stable within each of the four experimental blocks (Table 1 and Figures 1 and 2). The Friedman test provided additional support for this finding revealing that alpha power changed significantly over the four blocks (X2 (3)= 35.52, p <.001). Wilcoxon signed rank test demonstrated significant differences in alpha power between Reminisce I and Meditation I (T = 185.00, p =.003, r = .47), Meditation I and Reminisce II (T= 12.00, p =.001, r =.55), and Reminisce II and Meditation II (T = 210, p < .001, r = .62).

Table 1.

Mean, standard deviation, and median activity per spectral line measured in power across frequency bands and percent of data points within 25% of median.

Reminisce Meditation Reminisce Meditation
I I II II
Bands M (SD)
Median Percent within Stability Envelope
Theta (4–8 Hz) 5.73 (.95) 6.41 (2.61) 3.81 (.36) 4.63 (.42)
5.53 5.30 3.80 4.68
80% 45% 100% 100%
Alpha (8–13 Hz) 2.47 (.42) 3.48(1.21) 2.30 (.40) 4.71 (1.77)
2.40 2.89 2.20 4.39
95% 75% 85% 70%
Beta (13–30 Hz) 3.89 (.62) 4.33 (1.06) 3.37 (.61) 5.58(1.37)
3.91 4.27 3.44 5.23
95% 80% 95% 80%
Low Gamma (30–50 Hz) .38 (.03) .47 (.04) .48 (.05) .53 (.07)
.3825 .4804 .4785 .5161
100% 100% 100% 85%
High Gamma (70–120 Hz) .0292 (.002) .0291 (.003) .0254 (.003) .0312 (.003)
.0291 .0300 .0251 .0308
100% 100% 100% 95%
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Notes. The effects of meditation and reminiscing on direct cortical EEG recordings using an ABAB single case design. Mean activity per spectral band as measured in power (uV^2). Percent within Stability Envelope indicates what percentage of the data points within each condition fell within 25% of the median.

Figure 1.

Figure 1.

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The effects of meditation and reminiscing on direct cortical EEG recording using a ABAB single case design. Notes: Mean activity per spectral line as measured in power (uV^2) for theta (4–8 Hz), alpha (8–13 HZ), beta (13–30 HZ), low gamma (30–50 HZ), and high gamma (70–120 HZ) bands.

Figure 2.

Figure 2.

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Change in spectral power in individual bands over the four blocks and significant p values of Wilcoxon signed rank tests.

Visual analysis of the other bands (theta, beta, low gamma, high gamma) did not demonstrate both indicators of a possible causal relation between the introduction or removal of meditation as used during visual analyses (level and stability). Theta power did not display consistent level change between Reminisce I and Meditation I or data stability within Reminisce I or Meditation I. The Friedman test demonstrated that theta power changed significantly over the four blocks (X2 (3)= 33.06, p <.001) with significant differences found between Meditation I and Reminisce II (T= 3.00, p <.001, r = .60) and Reminisce II and Meditation II (T = 199, p < .001, r =.55), but not between Reminisce I and Meditation I (T = 132.00, p =.31, r = 0.021). Visual analysis suggested that beta power did not display consistent level change within Reminisce I and Meditation I, but did meet the stability criterion within all four blocks. The Friedman test found that beta power changed significantly over the four blocks (X2 (3)= 32.94, p <.001) with significant differences in power between Meditation I and Reminisce II (T= 19.00, p =.001, r = .51) and Reminisce II and Meditation II (T = 210, p < .001, r= .62), but not between Reminisce I and Meditation I (T = 210.00, p =.07, r =.28). Low gamma activity did not display consistent level change with the removal of the meditation task (Meditation I to Reminisce II), but did meet the stability criterion within the four blocks. The Friedman test found that low gamma power changed significantly over the four blocks (X2 (3)= 36.48, p <.001), demonstrating significant differences in low gamma power between Reminisce I and Meditation I (T= 207.00, p <.001, r = .60), but not between Meditation I Reminisce II (T= 110.00, p = .85, r =.03), or Reminisce II and Meditation II (T = 168, p = .02, r = .30). Finally, high gamma did not display consistent level change between Reminisce I and Meditation I, but did meet stability criterion over the four blocks. The Friedman test provided additional support for these findings: High gamma power changed significantly over the four blocks (X2 (3)= 26.16, p <.001) with significant differences in high gamma power between Meditation I and Reminisce II (T= 11.00,p <.001, r = .55), and Reminisce II and Meditation II (T= 208.00, p <.001, r = .61), but not Reminisce I and Meditation I (T = 113, p = .76, r = .04).

Discussion

This unique single case design study allowed for the evaluation of the effects of a brief breath awareness meditation on direct cortical EEG recording during an awake craniotomy. To evaluate a possible causal relation between the introduction or removal of meditation and change in spectral power, we conducted visual analyses of graphic displays of the data (Lane & Gast, 2014). To determine whether or not a breath awareness practice produced dramatic, replicable changes in behavior that last over time, we evaluated the level and stability of the spectral power for each band, for each of the four experimental blocks (Cooper et al., 2007). Secondary analyses included the Friedman test using the Wilcoxon signed rank test with adjusting Bonferroni-corrected alpha levels for posthoc analyses.

Our primary finding revealed that cortical activity in the alpha band consistently increased during a breath awareness meditation, when compared to a control state. Results are congruent with previous literature based on scalp EEG recordings that reported increased alpha during meditation (Dunn, 1999; Huang & Lo, 2009; Milz et al., 2014; Yu et al., 2011). Though less consistent, we also observed that when meditation was removed (Meditation I to Reminiscing I) theta, beta, and high gamma significantly decreased, and when meditation was again introduced the second time (Reminiscing II to Mediation II) theta, beta, and high gamma significant increased. Results may suggest practice effects. It may be that the due to the uniqueness of the situation (being asked to mediate during brain surgery), the first attempt at meditation was more difficult and of lower quality. After becoming familiar with the task in this unique setting, the participant may have been able to engage in a higher quality of practice.

This study provided a unique opportunity for greater insight into the physiology of meditation with less contamination of high-frequency muscle activity; however, the effects of a breath awareness meditation on gamma activity were inconclusive. Increased gamma activity and synchrony in scalp EEG during meditation in a meditator who was much more expert than ours has been observed (Lutz Greischar, Rawlings, Ricard, & Davidson, 2004). While it may be cortical in origin, more sophisticated analyses are needed to confirm this finding.

This study used a multiple-crossover ABAB single case design without randomization or blinding. iEEG data were recorded during a breath awareness meditation and an active control task in the operating room during an awake craniotomy for tumor resection. Results suggested that a brief breath awareness mediation was consistently associated with increased alpha power acquired from iEEG when compared to reminiscing. The ABAB single case design helped rule out anesthetic agents given prior to the reminiscence and meditation conditions as a cause of the frequency band changes. Single case design studies (Shadish & Sullivan, 2011) can be used whenever options for a randomized clinical trial with a moderate number of study participants may not be possible (Gabler, Duan, Vohra, & Kravitz, 2011).

Highlights.

  • A brief mediation was consistently associated with increased alpha power acquired from intracranial EEG.

  • Less consistent effects were found with theta, beta, and high gamma activity.

  • Intracranial EEG patterns may provide greater understanding into the physiology of meditation with less contamination.

Acknowledgments

The authors would like to acknowledge and offer gratitude the participant who made this study possible. We would also like to thank Dr. Ilker Yaylali, Aaron Kawamoto, Chris Timpa, and Dr. Lauren Simpson. This study was supported by Oregon Health and Science University and grants from the NIH (T32 AT002688 and K24 AT005121).

Footnotes

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