Does mindfulness training improve cognitive abilities? A systematic review of neuropsychological findings

Abstract

Mindfulness meditation practices (MMPs) are a subgroup of meditation practices which are receiving growing attention. The present paper reviews current evidence about the effects of MMPs on objective measures of cognitive functions. Five databases were searched. Twenty three studies providing measures of attention, memory, executive functions and further miscellaneous measures of cognition were included. Fifteen were controlled or randomized controlled studies and 8 were case–control studies. Overall, reviewed studies suggested that early phases of mindfulness training, which are more concerned with the development of focused attention, could be associated with significant improvements in selective and executive attention whereas the following phases, which are characterized by an open monitoring of internal and external stimuli, could be mainly associated with improved unfocused sustained attention abilities. Additionally, MMPs could enhance working memory capacity and some executive functions. However, many of the included studies show methodological limitations and negative results have been reported as well, plausibly reflecting differences in study design, study duration and patients' populations. Accordingly, even though findings here reviewed provided preliminary evidence suggesting that MMPs could enhance cognitive functions, available evidence should be considered with caution and further high quality studies investigating more standardized mindfulness meditation programs are needed.

Introduction

Mindfulness meditation practices (MMPs) are a subgroup of meditation practices which are receiving growing attention (Chiesa and Serretti, 2010, Ivanovski and Malhi, 2007). The word “mindfulness”, currently used to describe a particular way of paying attention to the present moment characterized by a receptive and non-judgemental attitude (Kabat-Zinn, 1994), derives from the Pāli word sati which can be originally found in the Abhidamma (Kiyota, 1978) and later in the Vishuddimagga (Buddhaghosa, 1976), a summary of the part of the Abhidamma that deals with meditation. Indeed, such term is frequently used to describe a particular type of meditation practices characterized by an open monitoring of present moment experiences which are usually separated and considered as a possible development of concentrative or “focused attention” meditations (Lutz, Slagter, Dunne, & Davidson, 2008).

The concept of mindfulness has its roots in Buddhist philosophy and MMP is a key element of several Buddhist meditations including Vipassana (Gunaratana, 1993) and Zen meditations (Kapleau, 1965). In the last decades mindfulness training has been widely incorporated into several clinically oriented group based meditation programs such as Mindfulness Based Stress Reduction (MBSR) (Kabat-Zinn, 1990) and Mindfulness Based Cognitive Therapy (MBCT) (Segal, Williams, & Teasdale, 2002). In addition, a number of psychological interventions including, among others, Dialectical Behavior Therapy (DBT) (Linehan, 1993) and Acceptance and Commitment Therapy (ACT) (Hayes, Strosahl, & Wilson, 1999), are usually considered as consistent with current conceptualizations of mindfulness and included among modern mindfulness based interventions (Baer, 2003). Note, however, that such interventions only partially incorporate formal meditation training and are characterized by significant differences as compared with other MMPs (Chiesa and Malinowski, submitted for publication, Rapgay and Bystrisky, 2009).

Of note, current evidence suggests that mindfulness training could have significant benefit on health, including reduced alcohol and substance consumption (Bowen et al., 2006), reduced blood pressure (Chiesa, 2009), decreased anxiety, depressive symptoms and relapses (Coelho et al., 2007, Kim et al., 2009) as well as significant benefits for patients suffering from various types of chronic pain (Chiesa & Serretti, in press), stress problems (Chiesa & Serretti, 2009), cancer (Ledesma & Kumano, 2009) and several further medical disorders (Chiesa & Serretti, 2010). Even though many studies on MMPs have been criticized for the lack of scientific rigor, including the lack of high quality randomized controlled studies designed to differentiate between the specific (i.e. specifically related to repeated sitting meditation practice) and the non specific (i.e. related to benefits' expectations) effects of such practices (Chiesa and Serretti, 2010, Toneatto and Nguyen, 2007) and the frequent use of self report instruments as measures of clinical improvements following mindfulness training (e.g. Chambers et al., 2009, Ivanovski and Malhi, 2007), overall available studies provide preliminary evidence for the clinical usefulness of such interventions.

It is noteworthy, however, that the bulk of studies investigating the clinical benefits of MMPs stands in stark contrast with the paucity of studies aimed at investigating more objective correlates of such practices, such as their effects on attention and other cognitive functions, at least up to recent years. On the other hand, as recent conceptualizations of MMPs consistently claim that they improve self regulation of attention (e.g. Bishop, Lau, & Shapiro, 2004; K. W. Brown and Ryan, 2003, Lau et al., 2006), the paucity of scientific studies investigating such issue is somewhat surprising and points out the need of a more thorough investigation and review of the cognitive correlates of mindfulness training. In addition, mindfulness meditation masters and instructors have frequently pointed to the benefits that MMPs could have on cognitive abilities, including attention, memory and other cognitive functions (e.g. Gunaratana, 1993, Kapleau, 1965, Teasdale et al., 1995), and such measures could provide empirical evidence concerning possible enhanced cognitive abilities associated with mindfulness training. Note also that significant psychological benefits linked to mindfulness training, including, among others, reduced cognitive reactivity (Raes, Dewulf, Van Heeringen, & Williams, 2009) as well as decreased avoidance and rumination (Kumar, Feldman, & C., H. S., 2008), could depend, at least initially, on the development of attentional control and inhibition of unnecessary elaborative processing (Baer, 2003, Bishop et al., 2004).

Accordingly, the aim of this paper is to review current evidence about the effects of MMPs on objective measures of cognitive functions, defined here in their broadest terms so as to include processes such as attention, memory and executive functions, and to provide a preliminary theoretical integration of reviewed findings. Critical issues concerning differences in the definition of mindfulness and current conceptualizations of cognition are explored, followed by a systematic description of the effects of MMPs on different domains of cognitive functions.

The state of mindfulness has frequently been described as a state of “presence of mind” which concerns a clear awareness of one's inner and outer worlds, including thoughts, sensations, emotions, actions or surroundings as they exist at any given moment (Gunaratana, 1993, Kapleau, 1965, Rahula, 1974). Accordingly, it has often been termed as “bare” attention (Gunaratana, 1993, Nyaniponika, 1973, Rahula, 1974), or alternatively as “pure” or “lucid” awareness (Das, 1997, Sogyal, 1992), emphasizing that mindfulness is supposed to reveal what is occurring, before or beyond conceptual and emotional classifications about what is or has taken place.

Unfortunately classical descriptions of mindfulness are usually somewhat poetic and abstract and they do not easily lend themselves to a scientific operationalization that could be used for scientific purposes on this topic. As a consequence, several authors have recently attempted to provide psychologically oriented definitions of mindfulness designed to overcome the difficulties related to early conceptualizations, emphasizing at least two points. The first component of mindfulness is usually referred to as a mental state characterized by full attention to internal and external experiences as they occur in the present moment (Bishop et al., 2004; K. W. Brown and Ryan, 2003, Kabat-Zinn, 1994). The second component is usually described as a particular attitude characterized by non judgment of, and openness to, current experience (Bishop et al., 2004; K. W. Brown and Ryan, 2003, Kabat-Zinn, 1994), which is supposed to lead to higher levels of exposure to negative stimuli and emotions (Kabat-Zinn et al., 1992) as well as to higher acceptance (Brown and Ryan, 2004, Hayes, 1994) and concurrent reduction of experiential avoidance (Hayes et al., 2004). Note, however, that significant discrepancies exist so far across current operational definitions of mindfulness (Baer et al., 2004, Baer et al., 2006; K. W. Brown & Ryan, 2003; A. M. Hayes and Feldman, 2004, Lau et al., 2006, Roemer and Orsillo, 2003).

In addition, it is noteworthy that several differences exist across different MMPs in terms of daily and total length of practice, types of meditation encompassed under the mindfulness “umbrella term” and specific instructions as to how the mindfulness state should be developed and maintained (for a comprehensive review see Lutz, Dunne, & Davidson, 2008). In sum, MMPs are currently delivered both as clinically oriented group based meditation programs, such as MBSR and MBCT, where mindfulness skills are usually taught over a period of 8 weeks and practitioners are asked to meditate for about 45 min daily (Kabat-Zinn, 1990, Segal et al., 2002), and as intensive retreats, where mindfulness techniques are practiced for 10 h or more daily (Forte et al., 1987–1988). Furthermore, the effects of mindfulness training have sometimes been explored as brief (e.g. 10 min) mindfulness-induction interventions (e.g. Erisman & Roemer, 2010). Although it has been pointed out that such interventions should be better labeled as brief “acceptance-based processing” (or with other labels that take into account the specific subcomponents of mindfulness treatments under investigation in each study) rather than “mindfulness training”, such brief laboratory manipulations have been considered as an important aspect of understanding how the cognitive system incorporates new information or procedures and what effects such change has (Williams, 2010).

Note also that in other cases mindfulness is operationalized as a dispositional mental trait (e.g. Brown & Ryan, 2003) which could have arisen through a complex interaction of genetic predisposition, environmental circumstances, and explicit training (Davidson, 2010) and which levels can vary both among different and within single individuals at different time points. It should be pointed out, however, that such different levels of dispositional mindfulness cannot be properly or easily attributed to specific mental training and they are thus systematically excluded from the present review. Nor this review addresses Langer's cognitive model of mindfulness (Langer, 1989, Langer, 1997), which includes alertness to distinctions, context, and multiple perspectives, openness to novelty, and orientation in the present (Sternberg, 2000), and usually involves working with material external to the participants, such as information to be learned or manipulated. Nevertheless, such mindfulness training, as Langer herself have explained (Langer, 1989), should be distinguished from other types of MMPs.

In addition to the issues outlined above, it is noteworthy that mindfulness (often referred to as open monitoring as well) training is usually associated with concentrative (or focused attention) training, such that in early stages of practice the monitoring faculty is needed to detect when mind wanders from the object onto which focused attention is directed, whereas in most advanced stages the practitioner gradually reduces the focus on an explicit object and the monitoring faculty is concurrently emphasized (Lutz et al., 2008, Lutz et al., 2008). Of further concern is the notion that, while in some cases the open monitoring faculty is seen as the final aim as well as the essence of practice, in other cases the open monitoring faculty becomes the basis that subsumes the development of a “reflexive awareness” as a means to understand the moment to moment flow of adaptive and maladaptive thoughts and feelings as well as their triggers and consequences (Lutz et al., 2008, Lutz et al., 2008, Rapgay and Bystrisky, 2009). Accordingly, in order to avoid discrepancies due to systematic differences in the underlying meditation practices, the present review is specifically concerned with cognitive substrates of mindfulness/open monitoring faculty either as a standalone intervention or as a development of prior focused attention meditation training.

Similar to the definition of mindfulness, there is no clear consensus as to how cognition and its constituents should be properly classified and categorized. Although an exhaustive overview of cognitive functions is out of the aims and possibilities of the present work, this section is aimed at exploring some of the main cognitive functions in order to provide a simplified theoretical framework that underpins our presentation of available findings about MMPs. In particular, we focused on attention, memory, and executive functions since they are the most represented ones in the studies included in this review.

Numerous theories have attempted to identify subcomponents of attention. One of the most consistent theoretical frameworks of attention suggests that it consists of three functionally distinct neural networks: alerting (also referred to as sustained attention or vigilance), orienting (or selective attention or concentration) and executive attention (or divided attention or conflict monitoring) (McDowd, 2007, Posner and Petersen, 1990, Posner and Rothbart, 2007). According to this model, alerting consists of achieving and maintaining a vigilant or alert state of preparedness, orienting regulates and limits attention to a subset of possible sensorial inputs, and executive attention prioritizes among competing thoughts, feelings, and responses (Posner, 2008, Posner and Petersen, 1990, Posner and Rothbart, 2007). In addition to these subsets of attention, the model suggested by Mirsky, Anthony, Duncan, Ahearn, and Kellam (1991) also includes shift of attention/attention switching referred to as “the ability to change attentive focus in a flexible and adaptive manner” (p. 112).

Memory is not a unitary process as well. Several types of partially independent memories, modulated by different brain regions, have been identified in both humans and animals (Budson, 2009, Henke, 2010). These memory types include, among others, semantic and episodic memory, procedural memory and working memory. This classification of memory systems evolved from the traditional dichotomy in the neuropsychological literature between long- and short-term memory. More in detail, all memory types mentioned above pertain to long-term memory, with the exception of working memory which brings together the fields of short-term memory and attention. The distinction between semantic and episodic memory, described for the first time by Tulving (1972), is essential to understand the existing difference between remembering the conceptual meaning of the word ‘pen’ (what is it? what is used for?) and remembering that in a specific time and place (for instance, during an experiment) we heard the word ‘pen’. In the first case we refer to our acquired general knowledge. In the second case we refer to our capacity to remember specific episodes. A completely different system is represented by procedural memory, which is linked to the acquisition and use of cognitive and behavioral skills, that are automatically retrieved and utilized in step-by-step procedures, such as when one rides a bicycle (Squire and Zola, 1996, Willingham et al., 1989). Finally, one of the most investigated memory systems is the one of working memory, which is assumed to be necessary for the maintenance of information in mind while performing complex tasks such as reasoning, comprehension and learning (Baddeley, 1986, Baddeley, 2010, Baddeley and Hitch, 1974). Working memory has traditionally been divided into three distinct components which are corroborated by imaging studies (Smith & Jonides, 1999): one processing and storing phonologic information, one processing and storing spatial information, and an executive system allocating attentional resources (Baddeley, 1998). Of note, memory can also be categorized in other ways, such as explicit versus implicit memory (Schacter, 1992, Squire and Zola, 1996) and verbal (Wagner et al., 1998) versus visual memory (Brewer, Zhao, Desmond, Glover, & Gabrieli, 1998).

Finally, under the label of executive functions are usually comprised higher-order cognitive abilities that facilitate the flexible modification of thought and behavior in front of novel cognitive or environmental demands. Executive functions include a number of abilities such as problem solving, planning, concept formation and decision making, attention and working memory that have been recently distinguished from emotional/motivational executive functions (Ardila, 2008). Among them, three core abilities have been reported to be clearly separable, even if moderately correlated with one another as well: information updating and monitoring, response inhibition (inhibitory control), and shifting (cognitive flexibility) (Miyake et al., 2000). In particular, information updating and monitoring capacities correspond to the above described executive component of working memory, whereas the other two executive functions are partially overlapping with attention models.

In conclusion, this brief overview highlights how summarized models of attention, memory and executive functions are not necessarily orthogonal in terms of either theoretical conceptualization or neural underpinnings (Gruber & Goschke, 2004). The reader should consider such interconnections in the evaluation of the following results.

As outlined above, both meditation practices in general and MMPs in particular encompass a large number of different practices. Taking into account the difficulties related to provide a comprehensive description of the specific traits of each MMP included in the present paper, the hypotheses of the present review will rely on one of the most consistent theoretical frameworks of meditation practices as elucidated by Lutz and colleagues (Lutz et al., 2008, Lutz et al., 2008). In sum, according to this model, the practice of mindfulness/open monitoring meditation is usually preceded and can be seen as the result of a sustained concentrative/focused attention meditation practice. This is consistent with historical accounts of meditation suggesting that concentrative attention should be mastered before receptive attention is cultivated (e.g. Kapleau, 1965), so as to avoid mind wandering and train the mind to be anchored to the present moment (Brown, 1977). According to Lutz et al.'s model (Lutz et al., 2008, Lutz et al., 2008), the practice of focused attention meditations involves the development of at least four different faculties, including sustained attention to a target object, monitoring faculty (so as to detect mind wandering), the ability to disengage from a distracting object without further involvement (attention switching), and the ability to redirect focus promptly to the chosen object (selective attention) (Lutz, Slagter, et al., 2008). As focused attention training advances, the well developed monitoring skill becomes the main point of transition into mindfulness/open monitoring practice, which is characterized by a gradual reduction of the focus on an explicit object and a concurrent monitoring of all present moment experiences without any explicit object (Lutz, Slagter, et al., 2008).

On the basis of this model one could hypothesize that early phases of MMPs could be mainly characterized by: (a) the development of conflict monitoring related to the continuous detection of mind wandering, (b) attention switching related to disengagement of distracting stimuli and redirection of attention to target objects, (c) selective attention related to the inhibition of cognitive processes different from the focus of concentration, and, as the practice advances, (d) increasing levels of sustained attention (I). On the other hand, most advanced stages of MMPs could be associated with further improvements of conflict monitoring and attention switching related to early detection and disengagement from distractions, and particularly to the development of unfocused sustained attention characterized by a more distributed attentional focus in comparison with early stages of practice (II). Additionally, even though both historical and modern conceptualizations of mindfulness have more rarely dealt with other cognitive functions, one could speculate that specific relationships could exist between MMP and (III) the development of working memory, which is closely related to several domains of attention (McVay and Kane, 2009, Redick and Engle, 2006), (IV) increases in memory specificity and meta-awareness, possibly related to the suppression of unnecessary elaborative processing (Bishop et al., 2004), and (V) executive functions such as measures of problem solving or verbal fluency, as a result of an improved ability to respond to external stimuli in more flexible rather than habitual reactive ways (e.g. Kabat-Zinn, 1990, Segal et al., 2002).