Elsevier

Neuropsychologia

Volume 51, Issue 13, November 2013, Pages 2581-2589
Neuropsychologia

Nosce te ipsum – Socrates revisited? Controlling momentary ruminative self-referent thoughts by neuromodulation of emotional working memory

https://doi.org/10.1016/j.neuropsychologia.2013.08.011Get rights and content

Highlights

  • Neuromodulation of the DLPFC enhances updating negative information in WM, as measured using the IST.

  • These WM operations mediate the effects of neuromodulation on self-referent ruminative thinking.

  • Trait rumination influences the effect of neuromodulation on self-referent ruminative thinking.

  • Cognitive self-regulation might help to control over streams of ruminative thoughts.

Abstract

It becomes ever more evident that cognitive operations serve as fundamental mechanisms underlying higher order ruminative thoughts. In this sham controlled within subjects study, we performed anodal transcranial Direct Current Stimulation (tDCS) over the left dorsolateral prefrontal cortex (DLPFC) in 32 healthy participants. We tested the causal hypothesis that the relationship between DLPFC activity and ruminative thinking is mediated by working memory operations. We used the Internal Shift Task, a paradigm in which participants have to update and shift between specific (non)emotional representations in working memory. Subsequently, during an unguided rest period approximately 20 min after the stimulation, we explored the occurrence of momentary ruminative self-referent thought. The results demonstrated that the influence of anodal tDCS of the left DLPFC (and not of sham stimulation) on momentary ruminative self-referent thinking is mediated by the enhancement of WM operations for angry faces. Moreover, the more individuals ruminate in everyday life (as measured using the Ruminative Response Style), the larger this mediation effect was. These findings suggest that enhancing cognitive self-regulation, by increasing the ability to update and shift away from negative representations in working memory, might help individuals to control unintentional streams of self-referent thoughts that are self-critical and self-evaluative, a thinking style known as rumination.

Introduction

We all spend time thinking about our own feelings, thoughts and behavior. Self-reflection enables us to create and clarify the meaning of past and present experiences (Boyd & Fales, 1983). This issue of self-referent thinking has ever inspired many scholars. Ancient philosophers have pondered on the nature and fundamental conditions of human self-focus as part of a greater understanding of personal identity. The classical aphorism “Nosce te ipsum” (Know thyself), attributed to Socrates, reflects the ultimate goal of using systematic self-questioning to increase one's self-knowledge and, as a result, to attain wisdom. However, although this process facilitates coping under a variety of circumstances (Austenfeld and Stanton, 2004, Pennebaker and Seagal, 1999, Trapnell and Campbell, 1999), it might turn out to be unconstructive when self-referent thoughts become rather abstract, evaluative and self-critical (e.g., “Why do I always react this way?”, Watkins, 2008). Moreover, self-referent thoughts might evolve in rumination – “a class of conscious thoughts that revolve around a common instrumental theme and that recur in the absence of immediate environmental demands requiring the thoughts” (Martin & Tesser, 1996, p. 7). Although these repetitive thoughts do not necessarily have unconstructive consequences (Watkins, 2008), depression vulnerable individuals have the tendency to focus their thoughts on negative information and personal concerns. It is therefore crucial to understand how self-evaluative ruminative thoughts can be regulated in order to prevent them from becoming unintentional and unconstructive, particularly in individuals who demonstrate a tendency to ruminate in everyday life.

Here, a fundamental question is whether the occurrence of ruminative thoughts could be attributed to underlying cognitive phenomena, such as information processing. In studies investigating this question, participants are usually required to make retrospective reports on the content of their usual thoughts, whether or not referring to a moment when they feel down, sad or depressed (e.g., Joormann et al., 2006, Joormann and Gotfib, 2008). These studies tap into stable dispositions of rumination, and have shown that these trait scores are associated with cognitive information processes such as working memory for negative information (i.e., angry faces) (De Lissnyder, Koster, Derakshan, & De Raedt, 2010). During everyday functioning, however, ruminative thoughts of healthy individuals fluctuate continuously from one moment to another (Moberly & Watkins, 2008). Therefore, it might be important to assess these thoughts as how they occur naturally. In a prior study, we looked into brain activation over a period of 8 min, and afterwards asked participants to report their momentary thoughts during this period. Results revealed that the more unwanted self-referent ruminative thoughts were present during the 8 min rest period, the less dorsolateral prefrontal cortex (DLPFC, Brodmann 9/46) activation was observed (Kühn, Vanderhasselt, De Raedt, & Gallinat, in press). Interestingly, the DLPFC seems not only involved in momentary ruminative thinking (e.g., Cooney et al., 2010, Kühn et al., 2013), but also in the active maintenance of attentional demands and contextual information during cognitive tasks (MacDonald et al., 2000, Ochsner and Gross, 2005) and cognitive control for mental representations in working memory (Barch et al., 1997, Braver et al., 2001, Braver et al., 1997, Curtis and D'Esposito, 2003, Goldmanrakic, 1994).

Working memory (WM) refers to a limited-capacity system to simultaneously maintain and select information over a short period of time in the service of current cognitive processes (Baddeley, 1992, Miyake et al., 2000, Smith and Jonides, 1999). The representations maintained in WM can be emotional or not, and the selection of information depends on its importance in the attainment of goals. In fact, it has been hypothesized that the relation between DLPFC and rumination would be mediated by WM operations (Joormann, Yoon, & Zetsche, 2007). In other words, the cognitive capacity to adequately update negative mental representations in WM, which is associated with DLPFC activation, might influence the occurrence of momentary self-referent thoughts, preventing these thoughts to become uncontrollable and unconstructive (e.g., rumination). This is in line with cognitive theories proposing that a reduced capacity to shift away from internal representations of negative information could be the functional process underlying the inability to control self-referent ruminative thoughts, which can result in a tendency to continuously ruminate over negative thoughts and feelings (e.g., Koster et al., 2011, Mor and Winquist, 2002, Watkins, 2008). Based on these models, we specifically hypothesized that momentary ruminative self-referent thoughts would be associated with WM processes to update and shift away from angry faces, an ability which is associated with the DLPFC.

To experimentally address this hypothesis, we used Transcranial Direct Current Stimulation (tDCS) which is a non-invasive neuromodulatory technique. This neuromodulatory technique consists of the application of a weak, direct electric current through electrodes positioned over one's scalp, which are able to reach the neuronal tissue and induce polarization-shifts on the resting membrane potential (Brunoni et al., 2011). Anodal stimulation generally facilitates cortical activity, whereas cathodal tDCS has opposite effects. In many previous studies it could already be demonstrated that tDCS of the left DLPFC enhances cognitive processes, both for non-emotional (e.g., Fregni et al., 2005, Leite et al., 2011, Mulquiney et al., 2011) as emotional processes (Boggio et al., 2007, Wolkenstein and Plewnia, 2013). In the current experiment, we used anodal left tDCS to causally modulate DLPFC neural activation in order to enhance WM operations, and subsequently explored the occurrence of self-referent ruminative thoughts. Based on the literature on cognitive deficits inrumination, we used the Internal Shift Task (IST, De Lissnyder, Koster, & De Raedt, 2012), an experimental paradigm to evaluate the ability to update and shift between specific emotional and non-emotional representations in WM (Chambers et al., 2008, Garavan, 1998). Twenty minutes after the end of the stimulation, we explored the occurrence of momentary ruminative self-referent thoughts during an unguided rest period. We asked individuals to rest without any specific task – which is known to result in a stream of undirected free thoughts – and self-referent ruminative thoughts – were assessed during this period using a short self-report questionnaire (subjects were not aware of the purpose of our study). In this paper, momentary self-referential ruminative thinking refers to a temporary cognitive thought pattern that is highly dependent on situational cues but that is independent of mood. Trait rumination, on the other hand, is defined as “behaviors and thoughts that focus one's attention on one's depressive symptoms and on the implications of those symptoms”, and is considered a habitual thinking response to sadness (Nolen-Hoeksema, 1991, p. 569).

Our study hypothesis is based on cognitive theories which propose that a reduced capacity to shift away from internal representations of angry faces (e.g., negative information) could be the functional process underlying the inability to control self-referent ruminative thoughts. Therefore, we hypothesized that the effect of anodal left DLPFC stimulation (versus sham) on momentary ruminative self-referent thoughts would be mediated by the influence of tDCS on WM operations to update and shift away from negative representations. Because the level of momentary self-focus is related to the habitual tendency to ruminate in everyday life (Moberly & Watkins, 2008), we predicted that trait rumination scores would moderate the relationship between neuromodulation, working memory operations for negative material and momentary ruminative self-referent thoughts.

Section snippets

Participants

Thirty-two right handed volunteers (20F/12M) ranging from 18 to 36 years in age (M=22.28, SD=3.74) participated in this study. All participants were university students or had a university degree and reported no history of depression or anxiety. The study was approved by the institutional ethics committee of the Mackenzie Presbyterian University, Brazil and by the National Ethics Committee (SISNEP, Brazil).

Trancranial direct current stimulation

Direct electrical current was applied by a saline-soaked pair of surface sponge rubber

Effects of tDCS on mood: analysis of variance

The two Stimulation (tDCS, sham)×Time (T0, T1,T2) repeated measures ANOVAs with positive and negative affects as dependent variable revealed a significant main effect of Time for PA, [F(2, 30)=17.86, p<.0001, ηp2=.54], and for NA, [F(2, 30) =6.82, p=.004, ηp2=.31]. Paired t-tests revealed that both in the sham and tDCS condition, participants reported less PA and NA towards the end of the experiment: T1 to T0 (p’s<.02) and T2 to T1 (p’s<.05). For both PA and NA, the main effect of Stimulation

Discussion

We investigated the influence of DLPFC neuromodulation on working memory (WM) operations and momentary ruminative self-referent thinking. Anodal tDCS of the left DLPFC (compared to sham) did not directly influence the occurrence of momentary ruminative self-referent thoughts. However, we observed that the influence of anodal tDCS (and not of sham stimulation) on momentary ruminative self-referent thinking was mediated by the enhancement of WM operations for angry faces. In other words, the

Acknowledgments

M.A.V. (FWO08/PDO/168) is a postdoctoral research fellow of the Research Foundation Flanders (FWO). Preparation of this paper was also supported by Grant BOF10/GOA/014 for a Concerted Research Action of Ghent University (awarded to R.D.R.). P.S.B. is supported by a CNPq researcher Grant (305718/2009-6). T.L. would like to thank the Research Foundation Flanders (FWO) for financial support (Grant G.0111.12).

References (61)

  • J. Joormann et al.

    Cognitive inhibition in depression

    Applied & Preventive Psychology

    (2007)
  • E.H.W. Koster et al.

    Understanding depressive rumination from a cognitive science perspective: The impaired disengagement hypothesis

    Clinical Psychology Review

    (2011)
  • A. Miyake et al.

    The unity and diversity of executive functions and their contributions to complex “frontal lobe” tasks: A latent variable analysis

    Cognitive Psychology

    (2000)
  • P.G. Mulquiney et al.

    Improving working memory: Exploring the effect of transcranial random noise stimulation and transcranial direct current stimulation on the dorsolateral prefrontal cortex

    Clinical Neurophysiology

    (2011)
  • K.N. Ochsner et al.

    The cognitive control of emotion. [Review]

    Trends in Cognitive Sciences

    (2005)
  • C. Papageorgiou et al.

    Treatment of recurrent major depression with attention training

    Cognitive and Behavioral Practice

    (2000)
  • J.M. Smith et al.

    A roadmap to rumination: A review of the definition, assessment, and conceptualization of this multifaceted construct

    Clinical Psychology Review

    (2009)
  • M.A. Vanderhasselt et al.

    How brooding minds inhibit negative material: An event-related fMRI study

    Brain and Cognition

    (2013)
  • L. Wolkenstein et al.

    Amelioration of cognitive control in depression by transcranial direct current stimulation

    Biological Psychiatry

    (2013)
  • J.L. Austenfeld et al.

    Coping through emotional approach: A new look at emotion, coping, and health-related outcomes

    Journal of Personality

    (2004)
  • A. Baddeley

    Working memory

    Science

    (1992)
  • A. Baddeley

    Working memory: Theories, models, and controversies

    Annual Review of Psychology

    (2012)
  • R.M. Baron et al.

    The moderator-mediator variable distinction in social psychological research: Conceptual, strategic and statistical considerations

    Journal of Personality and Social Psychology

    (1986)
  • E.M. Boyd et al.

    Reflective learning. Key to learning from experience

    Journal of Humanistic Psychology

    (1983)
  • R. Chambers et al.

    The impact of intensive mindfulness training on attentional control, cognitive style, and affect

    Cognitive Therapy and Research

    (2008)
  • R.E. Cooney et al.

    Neural correlates of rumination in depression

    Cognitive Affective & Behavioral Neuroscience

    (2010)
  • E. De Lissnyder et al.

    Emotional interference in working memory is related to rumination

    Cognitive Therapy and Research

    (2012)
  • E. De Lissnyder et al.

    The association between depressive symptoms and executive control impairments in response to emotional and non-emotional information

    Cognition & Emotion

    (2010)
  • R. De Raedt et al.

    Understanding vulnerability for depression from a cognitive neuroscience perspective: A reappraisal of attentional factors and a new conceptual framework

    Cognitive, Affective and Behavioural Neuroscience

    (2010)
  • M.S. Filler et al.

    Daydreaming as a function of cueing and task difficulty

    Perceptual and Motor Skills

    (1973)
  • Cited by (40)

    • A pilot randomized clinical trial of tDCS for increasing exercise engagement in individuals with elevated depressive symptoms: Rationale, design, and baseline characteristics

      2022, Contemporary Clinical Trials Communications
      Citation Excerpt :

      We were also unaware of support for similar effects in other regions, which would suggest an alternate neural target. We considered extracephalic cathode placement, as some studies have used [70,72], but chose the contralateral supraorbital location (as in Refs. [71,75] to avoid the potential for current flow across the brain stem. tDCS parameters (20 min at 1.0 mA) were chosen based published data and for consistency with parameters used in tDCS studies of cognitive control of emotion [68–73].

    • Combining top-down and bottom-up interventions targeting the vagus nerve to increase resilience

      2022, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      SuchSuch neuromodulation technique has been developed for home use, with remote supervision, facilitating treatment and making it a cost-effective intervention. TDCS applied to the prefrontal cortex has has been found capable to decrease intrusive stress-related thoughts (Vanderhasselt et al., 2013), but also decrease heart rate, increase HRV and possibly normalize parasympathetic functioning imbalance (Makovac et al., 2017). Brunoni and colleagues showed that in healthy participants, a single session of anodal tDCS applied to the left prefrontal cortex (as compared to sham or cathodal stimulation) led to an increase in vagally mediated control (Brunoni et al., 2013).

    View all citing articles on Scopus
    View full text