Meditation experience predicts negative reinforcement learning and is associated with attenuated FRN amplitude

Cognitive, Affective, & Behavioral Neuroscience (2019) 19:268–282 https://doi.org/10.3758/s13415-018-00665-0 Meditation experience predicts negative reinforcement learning and is associated with attenuated FRN amplitude Paul Knytl 1 & Bertram Opitz 1 Published online: 16 November 2018 # The Author(s) 2018 Abstract Focused attention meditation (FAM) practices are cognitive control exercises where meditators learn to maintain focus and attention in the face of distracting stimuli. Previous studies have shown that FAM is both activating and causing plastic changes to the mesolimbic dopamine system and some of its target structures, particularly the anterior cingulate cortex (ACC) and striatum. Feedback-based learning also depends on these systems and is known to be modulated by tonic dopamine levels. Capitalizing on previous findings that FAM practices seem to cause dopamine release, the present study shows that FAM experience predicts learning from negative feedback on a probabilistic selection task. Furthermore, meditators exhibited attenuated feedback-related negativity (FRN) as compared with nonmeditators and this effect scales with meditation experience. Given that reinforcement learning and FRN are modulated by dopamine levels, a possible explanation for our findings is that FAM practice causes persistent increases in tonic dopamine levels which scale with amount of practice, thus altering feedback processing. Keywords Feedback-learning bias . Feedback-related negativity . FRN . Reinforcement learning . Meditation . Dopamine . ACC . Striatum Since the turn of the century meditation has gone from relative obscurity in Western academia to explosive growth in interest and research. Only around 60 academic papers were published on the topic of mindfulness in 2003; by 2013 that number jumped to 600 (Shonin, Van Gordon, & Griffiths, 2013). The appeal is understandable; claimed benefits of meditation range from reduced stress (Kabat-Zinn, 2003) to improved immune function (Davidson et al., 2003), from improved attention and lower anxiety (Tang et al., 2007) to a novel treatment for depression (Teasdale et al., 2000), and has even been recommended as a possible way to manage symptoms of psychosis (Shonin, Van Gordon, & Griffiths, 2014). While some researchers have been pressing forward exploring the possible applications of meditation, others have been trying to understand what exactly is occurring in the nervous system during and after meditation, what systems are involved, and what the long-term effects of practice might be. In part due to methodological issues, inconsistent * Bertram Opitz 1 School of Psychology, University of Surrey, Guildford, Surrey GU2 7XH, UK operationalization, the relative lack of longitudinal studies, and the infancy of the field, the precise mechanisms and long- term effects of various meditation styles are still not entirely clear (Cahn & Polich, 2006; Hölzel et al., 2011; Tang, Hölzel, & Posner, 2015; Vago & Silbersweig, 2012). There has been recognition that effective study of these practices requires precise operationalization of the concept. The term meditation refers to a diverse group of cognitive practices which share some similarities and some fundamental differences (Lutz, Slagter, Dunne, & Davidson, 2008). To the uninitiated, the matter is further confused by the casual use of relevant terms by both the public and academia. For example, the term mindfulness can refer to a type of meditation, a trait, and a state of mind (Vago & Silbersweig, 2012). To address this, a framework has been introduced which categorizes meditative practices into three groups based on their primary cognitive strategy: focused attention meditation (FAM), openmonitoring meditation (OMM), and loving-kindness meditation (LKM; Hölzel et al., 2011; Lutz et al., 2008; Vago & Silbersweig, 2012). Of particular interest in the present study is FAM. FAM is central to many meditative traditions, such as Buddhist samatha and vipassana meditation and their derivative secular mindfulness practices and clinical interventions such as mindfulness-based stress reduction (MBSR), Cogn Affect Behav Neurosci (2019) 19:268–282 mindfulness-based cognitive therapy (MBCT), and other practices such as transcendental meditation (Harvey, 2015; Lutz et al., 2008; Vago & Silbersweig, 2012). FAM is characterized by the establishment, monitoring, and maintenance of attention on a chosen sensory object, such as the sensation of breathing (Lutz et al., 2008). What is striking about FAM is that the cognitive processes invoked during practice bear close resemblance to the processes that the brain’s mesencephalic dopamine system and its target areas are thought to perform. For instance, others have hypothesized that the continual establishment, monitoring, and reestablishment of attention on an object of meditation during FAM should elicit activity in those brain areas already associated with conflict monitoring and sustained attention, such as the dorsolateral prefrontal cortex (dlPFC) and the anterior cingulate cortex (ACC; Lutz et al., 2008). An early review of 12 neuroimaging studies of meditation found numerous brain areas active during meditation, such as the striatum, hippocampus, thalamus, along with the ACC and dlPFC (Cahn & Polich, 2006). As this review predates Lutz et al.’s (2008) operationalization, it does not directly specify what kind of meditation may be involved (FAM, OMM, LKM, etc.), even including some studies of Christian prayer. This inclusion of a wide range of practices involved in the reviewed studies may account for the diverse brain areas reportedly active in meditators. Studies looking only at practices having a clear FA component (e.g., Buddhist and secular mindfulness) consistently report brain areas involved in attention and conflict monitoring, including the dlPFC and particularly the ACC, to be reliably active in meditators (for a review, see Tang et al., 2015). There is also evidence of morphological differences and changes in plasticity in FAM practitioners. A recent anatomical likelihood estimation (ALE) meta-analysis of 21 morphometric brain imaging studies revealed higher grey and white matter density in the ACCs of meditators compared with nonmeditators (Fox et al., 2014). Neuroplastic changes may also happen relatively quickly after beginning FAM training; one intervention with an FAM component resulted in higher connectivity between the ACC and the brain stem after only 11 hours of practice (Tang et al., 2010). These findings suggest that meditation not only activates areas vital to attention but can also quickly induce neuroplastic growth in these brain regions. Neuroimaging studies have also revealed that the striatum, a core component of the dopamine system, is active during meditation. In one study, [11C]raclopride, a radio ligand that binds competitively with dopamine D2 receptors, had been used to measure participants’ dopamine tone in th (...truncated)