Spontaneous eye movements during focused-attention mindfulness meditation

RESEARCH ARTICLE Spontaneous eye movements during focusedattention mindfulness meditation Alessio Matiz ID1*, Cristiano Crescentini2, Anastasia Fabbro3,4, Riccardo Budai5, Massimo Bergamasco1, Franco Fabbro1,4 1 PERCRO Laboratory, Scuola Superiore “Sant’Anna”, Pisa, Italy, 2 Department of Languages and Literatures, Communication, Education and Society, University of Udine, Udine, Italy, 3 Department of Psychology, University of Rome La Sapienza, Rome, Italy, 4 Department of Medicine, University of Udine, Udine, Italy, 5 Department of Neuroscience, University-Hospital “S. Maria della Misericordia”, Udine, Italy * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Matiz A, Crescentini C, Fabbro A, Budai R, Bergamasco M, Fabbro F (2019) Spontaneous eye movements during focused-attention mindfulness meditation. PLoS ONE 14(1): e0210862. https:// doi.org/10.1371/journal.pone.0210862 Editor: Joseph Najbauer, University of Pécs Medical School, HUNGARY Received: May 25, 2018 Accepted: January 3, 2019 Abstract Oculometric measures have been proven to be useful markers of mind-wandering during visual tasks such as reading. However, little is known about ocular activity during mindfulness meditation, a mental practice naturally involving mind-wandering episodes. In order to explore this issue, we extracted closed-eyes ocular movement measurements via a covert technique (EEG recordings) from expert meditators during two repetitions of a 7-minute mindfulness meditation session, focusing on the breath, and two repetitions of a 7-minute instructed mind-wandering task. Power spectral density was estimated on both the vertical and horizontal components of eye movements. The results show a significantly smaller average amplitude of eye movements in the delta band (1–4 Hz) during mindfulness meditation than instructed mind-wandering. Moreover, participants’ meditation expertise correlated significantly with this average amplitude during both tasks, with more experienced meditators generally moving their eyes less than less experienced meditators. These findings suggest the potential use of this measure to detect mind-wandering episodes during mindfulness meditation and to assess meditation performance. Published: January 24, 2019 Copyright: © 2019 Matiz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Data are available from https://web.gin.g-node.org/muec79/EEG_ FAMvs.IMW. Funding: This work was supported by Scuola Superiore "Sant’Anna" (https://www.santannapisa. it/) Phd program to AM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Introduction Mindfulness meditation practitioners are skilled to intentionally sustain their focus on present-moment experiences (thoughts, emotions, feelings) with a detached attitude toward their mental contents. After an indefinite period of time, however, their minds usually drift away from the meditation object, giving rise to spontaneous thought. Sometime during this mental state, known as mind-wandering, which also extends for an indefinite period of time, practitioners become aware that they are not focused on the meditation object (e.g., breath) and try to shift their attention back to it. This cyclic process [1,2], between the two poles of being effectively engaged in a task and being off-task, appears to be common in all human activities [3]. It occurs to a degree that probably depends on task’s mental workload [4–6], task’s perceptual load [7] and on personal characteristics [8], and yet seemingly not on the type of task or its nature [9]. During disparate PLOS ONE | https://doi.org/10.1371/journal.pone.0210862 January 24, 2019 1 / 18 Spontaneous eye movements during focused-attention mindfulness meditation activities, the time spent in mind-wandering compared to the time occupied by effective task engagement seems to range from a 1:4 to a 1:1 ratio [8–11]. It is therefore fundamental to further understand the quality, utility and neural correlates of the mind’s duality of functioning, as well as to better detect when we are in one operational mode or the other. The basic detection method for mind-wandering episodes during task performance utilizes thought sampling. This method is based on requesting the subject to report his / her mindwandering whenever he / she realizes that his / her attention is off-task (self-caught mind-wandering), or intermittently interrupting the subject to ask about the content of his / her thoughts (probe-caught mind-wandering). Thought sampling methods enable the investigation of mind-wandering in terms of its frequency and content [12–14], in terms of the use or not of intentionality in its initiation and continuation [15], and in terms of its relation with individual characteristics [7,8,16–18], medical conditions [4,19] and its consequences on task performance [10,20–22]. Although mind-wandering has been linked to useful mental functions such as emotional processing [23], creative thinking [24] and autobiographical planning [12,14], it has also been related to reductions in task performance, which frequently occur during repetitive tasks [25–26]. Furthermore, neurocognitive markers of mind-wandering have been obtained through the observation of ERP and fMRI data. In this regard, it has been discovered that sensory-level cortical processing is reduced during mind-wandering episodes [27,28]. Moreover, distinct brain networks appear to be active during mind-wandering vs on-task performance, namely during rest or passive thought vs active cognitive processing, with the default mode network (DMN, including anterior and posterior cingulate cortices and medial prefrontal and parietal cortices) being particularly recruited during mind-wandering. These findings are consistent across a variety of tasks (for review, see [29]), including meditation [1]. Another neurocognitive marker of mind-wandering is represented by ocular activity. Indeed, one study that measured pupil diameter (PD) during working memory and reaction time tasks has provided further evidence for the reduction of sensory processing due to mindwandering [30]: task-evoked responses in PD were generally observed when the task required external focus and correct responses were produced, while spontaneous PD activity before stimulus presentation was linked to encoding failures and slower responses in the cognitive tasks. Eye movements, and also fixation duration, have been used as a measure of mind-wandering in individuals engaged in reading tasks, i.e. as a measure to detect mindless reading vs effective reading [11,31–34]. In other studies u (...truncated)