Neural correlates of focused attention and cognitive monitoring in meditation

Abstract

Meditation refers to a family of complex emotional and attentional regulatory practices, which can be classified into two main styles – focused attention (FA) and open monitoring (OM) – involving different attentional, cognitive monitoring and awareness processes. In a functional magnetic resonance study we originally characterized and contrasted FA and OM meditation forms within the same experiment, by an integrated FA–OM design. Theravada Buddhist monks, expert in both FA and OM meditation forms, and lay novices with 10 days of meditation practice, participated in the experiment. Our evidence suggests that expert meditators control cognitive engagement in conscious processing of sensory-related, thought and emotion contents, by massive self-regulation of fronto-parietal and insular areas in the left hemisphere, in a meditation state-dependent fashion. We also found that anterior cingulate and dorsolateral prefrontal cortices play antagonist roles in the executive control of the attention setting in meditation tasks. Our findings resolve the controversy between the hypothesis that meditative states are associated to transient hypofrontality or deactivation of executive brain areas, and evidence about the activation of executive brain areas in meditation. Finally, our study suggests that a functional reorganization of brain activity patterns for focused attention and cognitive monitoring takes place with mental practice, and that meditation-related neuroplasticity is crucially associated to a functional reorganization of activity patterns in prefrontal cortex and in the insula.

Introduction

Meditation can be conceptualized as a family of complex emotional and attentional regulatory practices, involving different attentional, cognitive monitoring and awareness processes. Many recent behavioral, electroencephalographic and neuroimaging studies have revealed the importance of investigating meditation states and traits to achieve an increased understanding of cognitive and affective neuroplasticity, attention and self-awareness, as well as for relevant clinical implications [7], [28].

Given that regulation of attention is the central commonality across the many different meditation methods [14], meditation practices can be usefully classified into two main styles – focused attention (FA) and open monitoring (OM) – depending on how the attentional processes are directed [7], [28]. In the FA (‘concentrative’) style, attention is focused on an intended object in a sustained fashion. The second style, OM (‘mindfulness-based’) meditation, involves the non-reactive monitoring of the content of experience from moment to moment, primarily as a means to recognize the nature of emotional and cognitive patterns.

FA meditation entails the capacities of monitoring the focus of attention and detecting distraction, disengaging attention from the source of distraction, and (re)directing and engaging attention to the intended object [28]. These attentional and monitoring functions have been related to dissociable systems in the brain involved in conflict monitoring, selective and sustained attention [12], [28], [32], [40]. A study with a binocular rivalry paradigm showed that Tibetan Buddhist monks were able to perceive a stable, superimposed percept of two dissimilar, competing images presented to separate eyes for a longer duration both during and after FA meditation, but not during and after a form of compassion (emotional OM) meditation [10]. These extreme increases in perceptual dominance durations suggest that extensive training in FA meditation might improve the abilities to sustain attention focus on a particular object and to control the flow of items being attended for conscious access. A recent fMRI study investigated the neural correlates of FA meditation in experts (following Tibetan Buddhist traditions) and novices, with meditation focus on an external visual point [4]. FA meditation compared with a rest condition, was associated with activation in multiple brain regions involved in monitoring, such as dorsolateral prefrontal cortex (DLPFC), attentional orienting (e.g., the superior frontal sulcus and intraparietal sulcus) and engaging attention (visual cortex). The meditation-related activation patterns depended on the level of expertise of the meditation practitioners.

OM meditation involves no explicit attentional focus, and therefore does not seem associated to brain areas implicated in sustained or focused attention, but to brain regions involved in vigilance, monitoring and disengagement of attention from sources of distraction from the ongoing stream of experience [28]. OM practices are based on an attentive set that is characterized by an open presence and a nonjudgemental awareness of sensory, cognitive and affective fields of experience in the present moment, and involves a higher-order awareness or observation of the ongoing mental processes [7]. The cultivation of this ‘reflexive’ awareness in OM meditation is associated to a more vivid conscious access to the rich features of each experience and enhanced metacognitive and self-regulation skills [28]. Behavioral studies have shown a more distributed attentional focus [39], enhanced conflict monitoring [37] and reduced attentional blink or more efficient resource allocation to serially presented targets [34] in OM meditation practitioners.

Despite the increasing number of studies on neural correlates of meditation states and traits, the differential brain activity patterns in focused attention and open monitoring meditation forms have not been contrasted yet in a neuroimaging experiment. Therefore, in an fMRI experiment we studied the FA and OM meditation-related brain activity patterns of Buddhist monks who are expert in Samatha (FA) and Vipassana (OM) meditation forms, and follow the oldest (Theravada) currently active Buddhist tradition. Vipassana (insight) meditation is central in mindfulness-based clinical interventions and studies [8], [38]. Although lay practitioners of Vipassana have participated in recent research (e.g., [17], [34]), to our knowledge this is the first study in which Theravada Buddhist monks are involved.

Our integrated FA–OM experimental design allows testing of whether FA and OM meditation styles enhance or, by contrast, reduce brain activations in frontal and other executive areas, given controversial evidence and theoretical stances. Indeed, it has been recently argued that meditative states are associated to transient hypofrontality or deactivation in executive networks [15], [26]. In contrast, other authors have emphasized the activation of executive areas in meditation [7], [28]. We hypothesize that the brain regions associated with conflict monitoring, such as the dorsal anterior cingulate cortex (ACC) and DLPFC [9], [40], selective attention, such as the temporal–parietal junction, ventrolateral prefrontal cortex, intraparietal sulcus and frontal eye fields [12] and sustained attention, such as right frontal and parietal areas, and the thalamus [13], [32], were more involved in inducing and maintaining the state of FA meditation as compared to the conditions of OM meditation and non-meditative rest [28]. Given neuropsychological [22] and psychophysical [18] evidence of dominance of the left cerebral hemisphere in conscious access, and theoretical bases to hypothesize a leading role of this hemisphere in conscious experiences [2], [22], [27], we predict a leftward bias of activation in fronto-parietal areas in OM meditation as compared to the other conditions.