Attending to the present: mindfulness meditation reveals distinct neural modes of self-reference
Abstract
It has long been theorised that there are two temporally distinct forms of self-reference: extended self-reference linking experiences across time, and momentary self-reference centred on the present. To characterise these two aspects of awareness, we used functional magnetic resonance imaging (fMRI) to examine monitoring of enduring traits (’narrative’ focus, NF) or momentary experience (’experiential’ focus, EF) in both novice participants and those having attended an 8 week course in mindfulness meditation, a program that trains individuals to develop focused attention on the present. In novices, EF yielded focal reductions in self-referential cortical midline regions (medial prefrontal cortex, mPFC) associated with NF. In trained participants, EF resulted in more marked and pervasive reductions in the mPFC, and increased engagement of a right lateralised network, comprising the lateral PFC and viscerosomatic areas such as the insula, secondary somatosensory cortex and inferior parietal lobule. Functional connectivity analyses further demonstrated a strong coupling between the right insula and the mPFC in novices that was uncoupled in the mindfulness group. These results suggest a fundamental neural dissociation between two distinct forms of self-awareness that are habitually integrated but can be dissociated through attentional training: the self across time and in the present moment.
Since William James’ early conceptualization, the ‘self ’ has been characterised as a source of permanence beneath the constantly shifting set of experiences that constitute conscious life. This permanence is often related to the construction of narratives that weave together the threads of temporally disparate experiences into a cohesive fabric. To account for this continuity, William James posited an explanatory ‘me’ to make sense of the ‘I’ acting in the present moment (James, 1890). Recently, progress has been made in characterizing the neural bases of the processes supporting William James’ ‘me’ in the form of ‘narrative’ self-reference (Gallagher, 2004), highlighting the role of the medial prefrontal cortices (mPFC) in supporting self awareness by linking subjective experiences across time (Neisser, 1997; Northoff and Bermpohl, 2004). The mPFC has been shown to support an array of self-related capacities, including memory for self-traits (Craik et al., 1999; Kelley et al., 2002; Fossati et al., 2003; Macrae et al., 2004), traits of similar others (Mitchell et al., 2006), reflected self-knowledge (Lieberman et al., 2004; Ochsner et al., 2005), and aspirations for the future (Johnson et al., 2006). As such, cortical midline processes may be characterised as supporting narrative self-reference that maintains continuity of identity across time (Gallagher, 2004).
Narrative self-reference stands in stark contrast to the immediate, agentic ‘I’ supporting the notion of momentary experience as an expression of selfhood. Most examinations of self-reference ignore mechanisms of momentary consciousness, which may represent core aspects of self-experience achieved earlier in development (Damasio, 1999; Zelazo and Frye, 1998; Gallagher, 2004) and may have evolved in earlier animal species (Panksepp, 2005). Indeed, little is known about whether the neural substrates underlying momentary self-reference are one and the same, or distinct from, cortical midline structures supporting narrative experience. One hypothesis suggests that awareness of momentary self-reference is neurally distinct from narrative self-reference and is derived from neural markers of transient body states, in particular, right lateralised exteroceptive somatic and interoceptive insular cortices (Damasio, 1999; Craig, 2004; Critchley et al., 2004). In the present study, we examined this thesis.
We investigated these hypothesised dual modes of self-reference by employing functional magnetic resonance imaging (fMRI) during attention to two temporally distinct foci of attention: the self as experienced across time and in the immediate moment. One obstacle to investigating present-centred awareness is the well-established tendency for the mind to wander and become distracted from the present moment in favour of temporally distant, stimulus-independent thought (SIT) (Smallwood and Schooler, 2006). SIT consists of automatically generated verbal or visual experiences (McGuire et al., 1996; Teasdale et al., 1995) akin to William James’ notion of a running ‘stream of consciousness’ (James, 1890), the basis of the narrative form of self-reference described above. SIT-related neural activation has been shown to reflect an automatic tendency to engage in narrative processes in the absence of a strong requirement to respond to external stimuli (McKiernan et al., 2006).
The theory of narrative generation as a default state of self-reference is increasingly supported by neural evidence: the cortical midline activity, which underlies narrative-generating mind wandering (Mason et al., 2007) is very similar to activity associated with the ‘default mode’ of resting attention (Gusnard et al., 2001; Raichle et al., 2001). This default mode suggests an endemic reliance upon the networks supporting temporally extended narrative processing, potentially obscuring recruitment of distinct networks for more immediate self-reflection. It may, therefore, be important to study individuals with specific training in monitoring moment-to-moment experience to more reliably recruit the brain regions supporting momentary self-focus in the face of a narrative generation bias. Mindfulness meditation is a form of attentional control training by which individuals develop the ability to direct and maintain attention towards the present moment (Kabat-Zinn et al., 1992; Segal et al., 2002). The current study examined individuals with mindfulness meditation training (MT) in addition to a novice group without such training, in an effort to determine whether the MT group would show an increased capacity to disengage from narrative generation and reveal the neural networks supporting present-centred self-awareness.
To characterise the brain regions supporting the hypothesised dual-modes of self-reference, participants were instructed to assume distinct modes of self-focus. Narrative focus (NF) calls for cognitive elaboration of mental events, thereby reducing attention towards other temporally proximal sensory objects. In contrast, experiential focus (EF) calls for the inhibition of cognitive elaboration on any one mental event in favour of broadly attending to more temporally proximal sensory objects, canvassing thoughts, feelings and physical sensations without selecting any one sensory object. As such, NF has been associated with increased ruminative thoughts about the self, while EF avoids rumination by disengaging attentional processes of self-referential elaboration (Watkins and Teasdale, 2001). In response to reading trait-related adjectives, participants in the present study were asked to engage either: (i) a NF mode, reflecting on what the adjective meant about them as a person or (ii) an EF mode, monitoring their moment-to-moment experience in response to the adjectives. Trait-related adjectives were chosen for their ability to promote self-reflection as evidenced by previous research (e.g. Fossati et al., 2003).