Cognitive-affective neural plasticity following active-controlled mindfulness intervention

Abstract

Mindfulness meditation is a set of attention-based, regulatory, and self-inquiry training regimes. Although the impact of mindfulness training (MT) on self-regulation is well established, the neural mechanisms supporting such plasticity are poorly understood. MT is thought to act through interoceptive salience and attentional control mechanisms, but until now conflicting evidence from behavioral and neural measures renders difficult distinguishing their respective roles. To resolve this question we conducted a fully randomized 6 week longitudinal trial of MT, explicitly controlling for cognitive and treatment effects with an active-control group. We measured behavioral metacognition and whole-brain blood oxygenation level-dependent (BOLD) signals using functional MRI during an affective Stroop task before and after intervention in healthy human subjects. Although both groups improved significantly on a response-inhibition task, only the MT group showed reduced affective Stroop conflict. Moreover, the MT group displayed greater dorsolateral prefrontal cortex responses during executive processing, consistent with increased recruitment of top-down mechanisms to resolve conflict. In contrast, we did not observe overall group-by-time interactions on negative affect-related reaction times or BOLD responses. However, only participants with the greatest amount of MT practice showed improvements in response inhibition and increased recruitment of dorsal anterior cingulate cortex, medial prefrontal cortex, and right anterior insula during negative valence processing. Our findings highlight the importance of active control in MT research, indicate unique neural mechanisms for progressive stages of mindfulness training, and suggest that optimal application of MT may differ depending on context, contrary to a one-size-fits-all approach.

Figure 1.

Affective Stroop trial scheme. A–C, Each row demonstrates an example of a single stimulus train for that level of task (passive view, A; congruent, B; and incongruent, C). IAPS images (third and fifth panels) were randomly selected from 40 negative, neutral, or positive images. Participants were instructed to count the “number of numbers” and to respond as quickly and accurately as possible following the second number display and before onset of the next trial. Response conflict is driven by incongruence between the Arabic numeral and the numeracy of the display (for details, see Materials and Methods).

Figure 2.

Behavioral results. A, Greater MT practice predicts increased EAT stop accuracy. Individual data points are change in percent stop accuracy (mean Time 2 minus mean Time 1) and total practice time for each participant. The MT practice versus SA slope is significantly greater than the SRL versus SA slope (F_(1,33) = 5.01; p = 0.032; data not shown above). Within the MT group (but not SRL) practice significantly predicted SA (p = 0.03; r = 0.52; linear regression line). B, Plot of group by time by task interaction. Values represent mean incongruent minus congruent (e.g., Stroop conflict) RTs across participants. MT (but not SRL) significantly reduced response conflict. Error bars indicate ±2 (SEM). See Results for details. *p = 0.03, t₍₁₈₎ = −2.43 (within group); **p = 0.02, F_(1,36) = 5.59 (group-by-time interaction). ns, Not significant.

Figure 3.

fMRI results. A, MT leads to greater left dorsolateral prefrontal cortex responses during task processing than in SRL. Post hoc analysis further revealed this effect to be driven by increases in the MT group. Top left, Sagittal image from SPM “glass brain,” which demonstrates spatial extent of activations throughout all slices of the brain simultaneously. The color bar indicates the t statistic associated with each voxel. A whole-brain statistical parametric map (in yellow) is displayed superimposed on sagittal, axial, and coronal views of the standard SPM T1-weighted template, for group by time interaction on the task (incongruent + congruent) > passive view contrast. p_FWE = 0.03 corrected on cluster level. The voxel selection threshold is p = 0.001. B, Positive correlation of MT practice and midcingulate cortex and premotor area activation during the task-by-emotion contrast. Post hoc analysis revealed this effect driven by positive correlations in the MT group. A whole-brain statistical parametric map (in yellow) for group by time interaction on the task > emotion contrast is displayed superimposed on coronal and sagittal sections of the SPM T1-weighted template. For the exploratory analysis, cluster selection is p = 0.01; p_FWE = 0.01.

Figure 4.

fMRI results. Greater levels of MT practice predict increased dorsolateral prefrontal (bottom left), right anterior insula (top right), and medial–prefrontal BOLD (bottom right) recruitment during negative emotional processing. Post hoc analysis further revealed this effect to be driven by positive correlations in the MT group. Top left, For visualization purposes, BOLD signal was extracted from the peak voxel (left posterior insula) of this contrast and plotted against practice minutes within MT group. The color bar indicates the t statistic associated with each voxel. A whole-brain statistical parametric map (in yellow) is displayed superimposed on coronal, sagittal, and axial views of the SPM T1-weighted template, for group by time interaction on the negative > neutral contrast. p_FWE < 0.05 corrected on cluster level. The voxel selection threshold is p = 0.001.