Mindfulness starts with the body: somatosensory attention and top-down modulation of cortical alpha rhythms in mindfulness meditation

Abstract

Using a common set of mindfulness exercises, mindfulness based stress reduction (MBSR) and mindfulness based cognitive therapy (MBCT) have been shown to reduce distress in chronic pain and decrease risk of depression relapse. These standardized mindfulness (ST-Mindfulness) practices predominantly require attending to breath and body sensations. Here, we offer a novel view of ST-Mindfulness's somatic focus as a form of training for optimizing attentional modulation of 7-14 Hz alpha rhythms that play a key role in filtering inputs to primary sensory neocortex and organizing the flow of sensory information in the brain. In support of the framework, we describe our previous finding that ST-Mindfulness enhanced attentional regulation of alpha in primary somatosensory cortex (SI). The framework allows us to make several predictions. In chronic pain, we predict somatic attention in ST-Mindfulness "de-biases" alpha in SI, freeing up pain-focused attentional resources. In depression relapse, we predict ST-Mindfulness's somatic attention competes with internally focused rumination, as internally focused cognitive processes (including working memory) rely on alpha filtering of sensory input. Our computational model predicts ST-Mindfulness enhances top-down modulation of alpha by facilitating precise alterations in timing and efficacy of SI thalamocortical inputs. We conclude by considering how the framework aligns with Buddhist teachings that mindfulness starts with "mindfulness of the body." Translating this theory into neurophysiology, we hypothesize that with its somatic focus, mindfulness' top-down alpha rhythm modulation in SI enhances gain control which, in turn, sensitizes practitioners to better detect and regulate when the mind wanders from its somatic focus. This enhanced regulation of somatic mind-wandering may be an important early stage of mindfulness training that leads to enhanced cognitive regulation and metacognition.

Keywords: alpha rhythm; attention; chronic pain; depression relapse; mindfulness meditation; somatosensory cortex; thalamocortical loop.

Figures

Figure 1

Summary of predictions on the effects of Standardized Mindfulness Training (ST-Mindfulness) on cognitive and clinical conditions through top–down alpha modulation. Green arrows—enhanced functions A → B: ST-Mindfulness enhances working memory (WM) (e.g., Jha et al., ; Van Vugt and Jha, 2011) and cued selective attention (e.g., Jha et al., ; for a related task, see also Jensen et al., 2012a,b). α → B: Top–down alpha modulation is associated with enhanced WM performance (e.g., Tuladhar et al., ; Jensen and Mazaheri, ; Van Dijk et al., 2010) and enhanced sensory perception in selective attention tasks (Kelly et al., ; Jones et al., ; Foxe and Snyder, 2011) with TMS studies suggesting alpha is causally implicated in memory (Sauseng et al., 2009) and perceptual tasks (Romei et al., 2010) A → α: ST-Mindfulness enhances attentional modulation of alpha rhythms in SI (Kerr et al., 2011a,b). Red arrows—reduced functions A → C: ST-Mindfulness reduces distress in chronic pain (e.g., Sephton et al., ; Gaylord et al., ; Schmidt et al., 2011) and reduces risk of depression relapse (e.g., Teasdale et al., ,; Segal et al., 2010). C → B: WM and selective attention performance are reduced in chronic pain (e.g., Gijsen et al., ; Moore et al., 2012) and depression (e.g., Goeleven et al., ; Roiser et al., 2012). Blue arrows—hypothesized mechanisms of ST-Mindfulness. Primary: A → α → C: We predict that 8-week ST-Mindfulness training elicits enhanced top–down alpha modulation in sensory cortex that corresponds to improved clinical conditions including chronic pain and depression. Secondary: A → α → B → C: We further predict that top–down alpa modulation after ST-Mindfulness for clinical conditions will be correlated with performance on cognitive measures including selective attention and working memory.

Figure 2

Thalamocortical circuitry involved in ST-Mindfulness and somatosensory attentional modulation of alpha rhythms. Attentionally driven increases in alpha rhythm power broadly suppress sensory throughput in the unattended area (via thalamocortical mechanisms); spatially specific suppression of alpha facilitates sensory throughput in the attended area from the sensory periphery to the thalamus and on to the cortex.

Figure 3

Alpha modulation and ST-Mindfulness training. (A) Compared to non-meditators, ST-Mindfulness subjects' exhibit greater alpha differentiation between attend-hand vs. attend-foot conditions in the early post-cue period [600–800 ms, indicated by shaded region; originally published in Kerr et al. (2011a,b). Permission to use figure received from Brain Research Bulletin]. (B) From two participants, illustration of SI localization, with equivalent current dipole (blue dots) overlaid on MRI brain structure images proximal to the omega shape in the anterior bank of the post-central gyrus.

Figure 4

Schematic illustration of computational neural modeling predictions on the origin of alpha. Green arrows represent excitatory synaptic connections and red circles inhibitory synaptic connections. We hypothesize that focal changes in alpha can be achieved by modulation of the lemniscal thalamic Ventral-Posterial medial (VPm_) pathway to SI, while diffuse regulation can be achieved through modulation of non-specific Ventral-Medial (VM) thalamic drive. The VM thalamic nucleus is under direct inhibitory control of the Basal Ganglia/Striatum circuit, which is influenced by the prefrontal cortex. These pathways suggests alpha modulation occurs through alteration of prefrontal-basal ganglia—thalamocortical circuits in ST-Mindfulness practitioners (see discussion in “Part-4: Predictions from our Computational Neural Model on Neural Mechanisms Underlying Enhanced Alpha Modulation in ST-Mindfulness,”).