Psychopharmacology DOI 10.1007/s00213-015-3926-x

ORIGINAL INVESTIGATION

Glucose and the wandering mind: not paying attention or simply out of fuel? L. H. W. Birnie 1 & J. Smallwood 2 & J. Reay 3 & L. M. Riby 1

Received: 5 July 2014 / Accepted: 24 March 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Rationale/objectives The impact of raising glycaemia by ingestion of a glucose drink has revealed cognitive facilitation, particularly for memory and attention. This study aimed to extend current knowledge by examining, for the first time, whether glucose load also moderates task-related (TRT) and task-unrelated thoughts (TUT) during activities that vary in their requirement for sustained attention. Method A 2 (25 g glucose vs. placebo) × 2 (fast vs. slow version of the Sustained Attention to Response Task (SART)) repeated measures, counterbalanced design was used with 16 healthy adults. Self-report questionnaires probed participants’ levels of TRT and TUT during SART performance. Prior to testing, the Short Imaginal Processes Inventory (SIPI) was also administered to help pinpoint the nature of thought processes during the task before and after treatment. Results Analysis of variance revealed no significant effect of treatment; however, we report a pattern of results that is consistent with glucose facilitation effects on task accuracy for more demanding attention tasks (d=0.56). Additionally, glucose improved the monitoring and task reflection as measured by TRT (d=0.33) in the more demanding task but no effect on TUT. Probing the nature of thought processes further, we also report two novel correlations (in the placebo) between fears of failure (indexed by the SIPI) and the number of TUT episodes

* L. M. Riby [email protected] 1

Department of Psychology, Northumbria University, Northumberland Building, Newcastle upon Tyne NE1 8ST, UK

2

Department of Psychology, University of York, York, UK

3

School of Social Sciences, Business & Law, Teesside University, Middlesbrough, UK

and perceived poor attention control (indexed by the SIPI) and number of TUT and speculate that glucose may act to buffer against TUT episodes under externally demanding situations. Conclusions These data extend previous research examining the glucose facilitation effect to the processing of internal thought processes. Keywords Glucose . Glucose ingestion . Mind wandering . Self-control . Attentional control . Executive function . Self-generated thought . Task-related thought . Task-unrelated thought . SART

Introduction The human brain uses glucose almost exclusively as its primary energy source and, since storage is limited, relies on a steady fuelling from our diet (Mark and Rose 1981; Parker and Benton 1995; Messier 2004 for mechanisms and pathways). Increasing blood glucose concentration has been found to enhance mental performance in a number of cognitive domains (for reviews Smith et al. 2011b; Riby and Riby 2006; Messier 2004; for meta-analysis Riby 2004). For example, the impact of glucose on cognitive performance has been observed in children (Lapp 1981); in adolescents (Smith et al. 2009, 2011a; Smith and Foster 2008); in younger- (Foster et al. 1998), middle- (Meikle et al. 2005; Riby et al. 2008a) and older-aged (Riby et al. 2004) adults; and in patient groups with mild cognitive impairment (Riby et al. 2009), dementia (Manning et al. 1993) and schizophrenia (Stone et al. 2005). The special status of glucose in cognition is also highlighted in studies examining raised blood glucose in disease. For example, abnormalities in glucose regulation have been found to moderate cognitive performance in diabetes (Jones et al. 2014; Smith et al. 2014). Those cognitive processes that are

Psychopharmacology

particularly susceptible to the glucose action typically satisfy one or more of the following three conditions: they (1) involve numerous memory operations, (2) place large demands on cognitive resources and/or (3) involve controlled executive processes in the brain. As an example of condition 1 being satisfied, glucose-mediated cognitive facilitation is more pronounced in memory tasks that involve the retrieval from declarative memory (verbal episodic effect size d=0.91; semantic d=0.73) and working memory (d=0.49; Riby 2004). Similarly, during difficult or demanding cognitive activities, increasing resources by a glucose-containing drink have proven beneficial (Kennedy and Scholey 2000). In addition, performing traditional assessments of frontal executive function (Benton et al. 1994; Brown and Riby 2013), coordinating dual tasks rather than single tasks (Scholey et al. 2014) and brain markers of frontal executive processes (fMRI Stone et al. 2005; EEG Riby et al. 2008b) have all been found to benefit from fuelling the brain with glucose. Whilst research has examined the glucose action in relation to the processing of external events, the impact of glucose on the processing of internal trains of thought has been neglected. However, an emerging field associating glucose as a limited energy resource to an individual’s self-control of thought processes is informative here. Baumeister and colleagues (e.g. 2011) have suggested that sufficient supply of glucose to the brain is critical for activities involving self-control and the management of thoughts, emotions and behaviour. It is argued that the capacity for self-control draws on effortful controlled executive, rather than automatic, processes, and for this reason alone, it is hardly surprising that increasing glycaemia is beneficial, given the above-mentioned evidence related to task demands and external task performance (Baumeister et al. 2000). Gailliot et al. (2007) carried out a series of experiments that systematically examine the link between self-control of thoughts, emotions and subsequent behaviour (e.g. controlling thoughts of dying, suppression of stereotypical and prejudiced thoughts) and argued strongly for a “shortage of fuel” account to explain difficulties in self-control since glucose ingestion redresses the balance and improves self-regulation of behaviour. Although a recent meta-analysis on the topic has found a large effect size (d=0.75) of glucose ingestion on “ego-depletion” and self-control (Hagger et al. 2010), the findings have been criticised on methodological grounds. Lange and Eggert (2014), using more powerful research designs, failed to replicate earlier work and as a consequence should be consulted during the planning of future experimental work. Regardless of the discrepancies in research findings, similarities can be seen between this aspect of behavioural work, managing thoughts and controlling the self and the monitoring of stimulusindependent thought studied here. The current study explored the effect of glucose on the control of self-generated thoughts in the context of a task in which sustained external processing is important. Experiences such as

daydreaming or mind wandering arise through a process whereby thoughts and feelings are generated independent of events taking place in the external environment. Current accounts of self-generated thought suggest that the phenomenon depends upon understanding what causes the trigger, or onset, of the experience as well as processes that control the maintenance of internally generated information in consciousness (Smallwood 2013; Smallwood and Schooler 2015). In general, self-generated thoughts can been linked to beneficial outcomes, such as planning (Baird et al. 2011), self-memory (Smallwood et al. 2011), delayed gratification (Smallwood et al. 2013), reduced stress (Engert et al. 2015) and creativity (Baird et al. 2012). However, when these experiences occur in a demanding task, they can derail performance because the self-generated experiences monopolise limited attentional resources leading to poor comprehension (Smallwood et al. 2008b) and difficulties in sustained attention (Smallwood et al. 2004). The absent-minded lapses that occur during self-generated thought arise because of the reduction in processing of sensory information that occurs when the mind wanders (Smallwood et al. 2008a; Barron et al. 2011). This state of perceptual decoupling is thought to occur because neural populations in sensory cortices show reduced phase locking to input reducing the strength of cortical responses to external input (Baird et al. 2014). A recent meta-analysis has shown the reliability of the negative consequences of self-generated thoughts that occur during mind wandering on ongoing task performance (Randall et al. 2014). Importantly, although self-generated thoughts tend to be least frequent in externally demanding tasks, it is argued that in these situations, it is most damaging to external task performance; this is known as the context regulation hypothesis (Smallwood and Andrews-Hanna 2013). To the best of our knowledge, no study has investigated the impact of increasing the provision of glucose to the brain on our ability to manage the context in which mind wandering episodes occur and in particular the behavioural consequences of self-generated thoughts (operationalised here as taskunrelated thought (TUT); however, see Riby et al. 2014 on glucose regulation). To enable a comprehensive account of thought patterns during task, we also consider thoughts related to the current activity (task-related thoughts (TRT)). Using a novel combination of the thinking component of the Dundee Stress State Questionnaire (DSSQ; a measure of TUT and TRT; Matthews et al. 1999), the Short Imaginal Processes Inventory (SIPI; a measure to pinpoint the nature of mind wandering episodes, e.g. the result of poor attentional control) and a cognitive task (Sustained Attention to Response Task (SART); Robertson et al. 1997), this study aimed to investigate whether increasing blood glucose could alter reports of TUT and TRT during a (i) demanding and (ii) relatively less demanding task. A further aim was to uncover which specific characteristics of mind wandering are influenced by increasing glycaemia. There were three specific questions: (1) Given

Psychopharmacology

that glucose has been purported to provide additional cognitive resources, does additional cognitive control derived from glucose load impact on TUT and TRT frequency, and is this influenced by the difficulty of the primary task? (2) Are specific contents of mind wandering episodes that are especially negative (indexed by the SIPI; e.g. fear of failure, perceived poor attentional control) related to the pattern of TUT, TRT and behaviour, particularly after glucose treatment? (3) Consistent with the research examining external task performance, would increased behavioural performance on the cognitive task (particularly the more demanding version) emerge after glucose treatment?

Methods Design and treatments Participants took part in two separate counterbalanced conditions using the same mixing and sweetness matching procedure which has demonstrated the glucose facilitation effect in previous research (e.g. Riby et al. 2008; Meikle et al. 2004): Glucose treatment—25 g glucose dissolved in 200 ml water flavoured with 30 ml “no added sugar” orange squash Placebo—200 ml water flavoured with four saccharin tablets and 45 ml “no added sugar” orange squash

theoretical constructs corresponding to participants’ inner experiences. The SIPI scored participants on three subscales—(1) positive-constructive daydreaming—belief that daydreams are worthwhile, solve problems, help generate original ideas, are stimulating, leave warm feelings and generate pleasant thoughts; (2) guilt and fear of failure daydreaming—has daydreams with depressing, frightening, panicky qualities; and (3) poor attentional control daydreaming—tendencies toward mind wandering and drifting thoughts. The SIPI consists of statements such as “I tend to be quite wrapped up and interested in whatever I am doing”. This was then followed by five boxes, numbered 1–5. The meanings were explained before the questionnaire statements, number 5 stands for “very true or strongly characteristic of me”, whilst number 1 stands for “definitely untrue or strongly uncharacteristic of me”. Participants were required to select the appropriate option they felt described them best given the statement. The thought probe used was the thinking component of the Dundee Stress State Questionnaire (DSSQ; Matthews et al. 1999) which is a 16-item questionnaire that records a retrospective measure of a participant’s TRT and TUT after a recently completed task. This component is divided into two separate eight-item sections. The first eight items correspond to TRT, and the second eight items correspond to TUT. Typical items corresponding to TRT included “I thought about the purpose of this task”. Items corresponding to TUT included items that state questions such as “I thought about something that may happen in the future”. Each participant was given a 16-item DSSQ after each block and session (i.e. placebo vs. glucose). Each response was measure on a 5-point Likert scale ranging from “never” to “very often”.

Participants The Sustained Attention Task Sixteen adults between the ages of 18 and 45 years participated (eight females; mean age=23.7 years, SD=5 years). All had normal or corrected to normal vision and during screening reported no neurological or physical conditions that may hinder attention or affect task performance. Participant exclusion criteria also included self-reported impaired fasting status, impaired glucose tolerance or diabetes. Participants were opportunistically recruited from the student population of Newcastle upon Tyne, and no financial reward was given for taking part in the experiment. Ethical approval was obtained from the Department of Psychology Ethics Board at Northumbria University. All participants gave written informed consent prior to participation. Materials Pre-testing self-reported perception of daydreaming The Short Imaginal Processes Inventory (SIPI; Huba et al. 1982) was used to enable participants to self-assess how much their minds wander as part of their daily functioning. The SIPI was suitable for the current study as it consisted of three relevant

This study employed the SART (Robertson et al. 1997) that was designed to test participants’ attentional capabilities. The test required participants to both respond to frequent relevant stimuli and inhibit their response when they see an infrequent target. The SART used during the current study was modified to present stimuli at two set speeds as research has demonstrated that if stimuli on the SART are presented quickly, the amount of task-unrelated episodes is comparatively lower than if stimuli are presented slowly (Giambra 1995). In addition to providing a manipulation which would increase/decrease the likelihood of mind wandering, by altering task demands, we could seek to replicate previous cognitive task research suggesting more demanding tasks benefit from increasing blood glucose. The modified SART programme chosen for this experiment included an X or Y stimuli (both of which followed a small crosshair to focus participants’ visual alignment upon the stimuli). Participants were given the following instruction before the test: “In this task you will see the letters X and Yappear on the screen. Your task will be to push the space bar whenever you see the letter X. Do

Psychopharmacology

nothing when the letter Y appears on the screen”. The X and Y were consistent in size both measuring 1 cm2, and both stimuli were black whilst being presented on a white background. In a practice phase, ten sample stimuli were presented in a 9/1 ratio (X/Y). The experimental phase consisted of six blocks. Three of the blocks last approximately 1 min and 55 s (65-stimulus cycle) of testing with a 52/13 ratio (X/Y), whilst three of the blocks consisted of 4 min and 40 s (65 stimuli cycle) of testing with a 52/13 ratio (X/Y). The testing programme varied the presentation order of these blocks. During both types of block, the fixation crosshair was present for 900 ms and both blocks had target stimuli present for 300 ms. The difference between the blocks was the stimulus presentation rate, with the shorter block period’s stimuli having a 500-ms delay (difficult version), whilst during the longer block, stimuli contained a 3000-ms delay (easy version) between presentations. After each block, participants were asked to complete the thinking component of the DSSQ. Procedure Each participant attended two separate 40-min laboratory visits; on the first visit, after reading the participant information sheet and giving informed consent, they ingested one of the independently mixed solutions, and on their follow-up visit, they ingested the other solution. Before attendance at each of the two sessions, participants were instructed to fast for 2 h (see Riby 2004 for discussion of fasting regime). During the first session, the SIPI questionnaire was administered. After use of the counterbalance measures to determine which solution (placebo or treatment) the participant would be administered, the experimenter waited for 15 min postadministration until the test began. All participants followed the same procedure. Following the 15-min ingestion period, participants were given clear instructions involving task completion; during this, they were told they would complete the SART task, and at predetermined points, the test would pause and they would be asked to complete a DSSQ. The task took approximately 25 min, after which participants were asked to attend a follow-up test (approximately 1 week later) under the same conditions at a date of their convenience. After the end of the second visit, participants were then fully debriefed.

out on the frequency of TRT during the SART. The main effects were not significant (p values >0.05). The interaction between treatment and speed approached significance (Wilks’ lambda=0.83, f(1, 15)=3.0, p=0.066). The treatment difference occurred when stimuli were presented at the faster rate of 3000 ms, which is arguably where more monitoring of performance is required (see Table 1 for scores collapsed across blocks). To further explore the trend, we completed two paired samples t tests. The first confirmed a significant difference between slow (49.3) and fast (54.7) speeds in the glucose condition (t(15)=2.469, p=0.026), and the second revealed no difference between slow (48.4) and fast (49.3) speeds in the placebo condition (t(15)=0.420, p=0.68). This finding suggests that glucose allowed more task-related thoughts during the fast condition relative to the slow condition (d=0.33). TUT A 2 (treatment) × 2 (speed) repeated measures ANOVA was carried out on the frequency of TUT during performance of the SART. The main effect of speed was significant demonstrating a successful task difficulty manipulation in that participants experienced more TUT during blocks of testing when the presentation rate of stimuli was slower (3000 ms= 46.6 vs. 500 ms=36.6; Wilks’ lambda=0.54, f(1, 15)=12.8, p=0.003). All other effects were not significant (p values >0.05). The effects of glucose on SART task performance Correct response hits to frequent stimuli Hit rate on the SART was analysed using a 2 (treatment) × 2 (speed) repeated measures ANOVA. The main effects were not significant (p values >0.05). The interaction between treatment and speed of stimulus presentation approached significance (Wilks’ lambda=0.83, f(1, 15)=3.2, p=0.096). Since performance approached ceiling across all conditions and only a statistical trend was observed, we need to be cautious with this finding. However, we predicted facilitation for the more difficult (fast) condition evident in Table 1; therefore, we calculated Cohen’s d to allow comparison with previous studies examining the task domains that may benefit from the glucose action (d=0.56; medium effect).

Results False alarms to infrequent stimuli The effects of glucose on the frequency of TRT and TUT during task TRT A 2 (treatment: glucose vs. placebo) × 2 (speed: slow vs. fast) repeated measures analysis of variance (ANOVA) was carried

Traditionally, the false alarm measure has been used as the primary index of behavioural performance (e.g. Greer et al. 2013). Testing demonstrated a significant effect of speed of stimulus presentation on false alarm rates (Wilks’ lambda= 0.21, f(1, 15)=55.7, p<0.001). Table 1 highlights that false alarms occurred more frequently during the fast (14.4 vs. 7.2),

Psychopharmacology Table 1 Means (SDs) of participants’ TUT and TRT scores during both fast and slow stimulus presentation rates on the SART task across placebo and glucose treatments

Treatment

SART speed

TUT score

TRT score

Accuracy

False alarms

Reaction time

Placebo

Slow Fast Slow Fast

46.9 (20.7) 38.2 (17.4) 46.3 (19.1) 35.1 (18.1)

48.4 (16.0) 49.3 (13.9) 49.3 (16.7) 54.7 (18.5)

98 (3.8) 98 (2.3) 98 (2.7) 99 (1.0)

7.4 (4.6) 14.8 (6.7) 6.9 (5.2) 14.0 (7.5)

340.0 (38.2) 317.5 (46.8) 351.3 (46.7) 322.7 (36.9)

Glucose

more difficult blocks of testing. The main effect of treatment and the interaction were not significant (p>0.05). Mean reaction time Mean reaction time on the SART was analysed using a 2 (treatment) × 2 (speed) repeated measures ANOVA. The main effect of the speed of stimulus presentation was significant demonstrating quicker responding at the faster stimulus presentation rate (Wilks’ lambda=0.37, f(1, 15)=25.4, p<0.001). All other effects were not significant (p values >0.05). Correlational analysis of DSSQ and SIPI scores Pearson’s correlation showed a strong positive relationship between participant’s total DSSQ TUT scores across the entire session who had been administered the placebo and their scores on the guilt and fear of failure daydreaming component on the SIPI (r=0.61, p=0.013; see Fig. 1). After glucose, this correlation was not significant (r=0.35, p=0.179). Fisher’s r to z transformations to test the significance of the difference between the two dependent correlations reveal no significant difference (z=0.88, p=0.38). After placebo treatment, Pearson’s correlation also highlighted a strong positive relationship between participants’ total DSSQ TUT scores and their scores on the poor attentional control scale on the SIPI (r=0.62, p=0.010; see Fig. 1). Again, after glucose, this correlation was not significant (r=0.29, p=0.272). This suggests that participants who experience poor attentional control and drift off into taskunrelated thought can seek to buffer this occurrence by taking glucose. Fisher’s r to z transformations to test the significance of the difference between the two dependent correlations reveal no significant difference (z=1.09, p=0.272). The correlations between TUT and the positiveconstructive daydreaming component of the SIPI and the correlations between TRT and all of the SIPI components were not significant (all p>0.05).

Discussion The present study investigated the impact of glucose ingestion on subjective reports of mind wandering and subsequent behavioural consequences whilst participants performed a

Sustained Attention Response Task (SART). Consistent with the context regulation hypothesis, we anticipated participants to be more task focussed during the more difficult condition because of the need for greater external attention. In line with this position, we found that retrospective reports of TUT were higher during the relatively undemanding version of the task. Critically, we found evidence that glucose facilitated superior focus in the externally demanding task by increasing the amount of TRT that participants reported during the more difficult condition. We interpret this finding as glucose providing the additional fuel to enable the effective control and monitoring of performance when task demands are high. Indeed, the TRT measure is composed of items such as “I thought about how much time I had left” and “I thought about my level of ability”. This level of monitoring, rather than being distracting, may reflect the potential benefits that meta-awareness of conscious experience might bring (Schooler 2002; Schooler et al. 2011), an interpretation that is supported by our prior EEG work. Riby et al. (2008c) identified a central negativity event-related potential component which was enhanced in individuals experiencing high levels of TRT as well as evidence that the P3a component was moderated by glucose ingestion. The P3a component has been shown to increase when attention is monitored (Polich and Criado 2006). Finally, these data mirror findings that external task performance requiring frontal executive processes can benefit from increased provision of glucose to the brain (e.g. Brown and Riby 2013). Based on these results, we propose that glucose is important in the context regulation of cognition by increasing a participant’s tendency to monitor the contents of their thoughts. In addition to glucose enhancing TRT, behavioural performance during the faster presentation rate, SART accuracy was enhanced (d=0.56). This moderate effect size for the SART performance is comparable to the overall average effect size reported for the glucose facilitation effect (d=0.56 extracted for 104 studies; Riby 2004) and is consistent with the abovementioned task difficulty account. These data should be treated with caution given that the difference is a statistical trend only and the finding that hit rates approached ceiling performance. However, we argue that the glucose effect is underestimated as the ceiling performance gives little opportunity for enhancement. The TRT and SART accuracy data are consistent with condition 2 (task difficulty) highlighted previously as a critical moderator of the glucose facilitation effect.

Psychopharmacology

Placebo

Glucose

Placebo

Glucose

Fig. 1 Task-unrelated thought (collapsed across blocks and task difficulty/speed) during the SART task and the relationship between perceived attentional control and fear of failure and guilt

In more demanding task conditions, the additional resource provided by glucose bolsters performance and task monitoring functions. Subjective reports of task difficulty and increasing the complexity of the task (e.g. increasing working memory load or adding a dual task) have both been associated with reliable glucose facilitation elsewhere (Kennedy and Scholey 2000; Scholey et al. 2014). It is worthwhile noting the false alarm data was not consistent with this view; however, because task difficulty was manipulated by speed of presentation, it is possible that the false alarm rate in part reflects the fact that failure to respond is less likely to occur when the window of opportunity for responding is lengthened. More relevant to the aims of the current investigation is our analysis of perceived mind wandering inherent in the

individual. The SIPI questionnaire is an ideal tool to investigate general ability of attentional control and level of distractibility, more negative daydreaming such as a fear of failure and also what we believe as more positive daydreaming such as bolstering problem-solving ability (Baird et al., 2012). Correlational analysis indicated a significant, positive relationship between TUT scores under the placebo condition and scores on the guilt and fear of failure daydreaming scale score. For those individuals who suffer increased rumination of a negative manner (e.g. fear of failure), it is not unreasonable to suggest greater task-unrelated thoughts during performance. When participants consumed glucose, the relationship was found to be non-significant (note the difference between placebo and glucose correlations was not significant). Although these data are

Psychopharmacology

correlational, we hypothesise that they may reflect the bolstering effect that glucose may have in terms of an increased focus on the task in hand, an observation that complements prior studies linking glucose to self-control and emotion regulation, and not specifically to mind wandering (Gailliot and Baumeister 2007). This would be consistent with the effect of glucose effects on mood (Benton 2002) and the findings that negative mood states heighten mind wandering episodes that are focused on the past (Smallwood et al. 2009; Smallwood and O’Connor 2011). Although this was not a primary aim of this investigation, these results support the content regulation hypothesis (Smallwood and AndrewsHanna 2013) that proposes individuals engage in control processes to steer their self-generated thoughts away from negative and unpleasant topics. Under these circumstances, glucose may provide the additional resources to allow controlled processes to be engaged. Together, these results suggest that glucose metabolism may be important in the capacity of the executive system in mediating the context in which mind wandering occurs and the content of the episodes. This corresponds favourably with research conducted by Benton et al. (1994) who found increased attentional capabilities in participants who were administered glucose prior to testing in comparison to the control group and also increased attentional resource whilst dividing attention (Scholey et al. 2009). Furthermore, this finding seems to support research suggesting that if a person is suffering from a deficit in blood glucose, then they will show impaired cognitive functioning, including being less able to focus attention on a perceptual input from external stimuli. This is supported by the current findings as glucose did not correlate with TUT scores, with glucose seemingly serving a buffer function, whereas the placebo condition showed a correlation with TUT scores. To conclude, by measuring three traits of mind wandering, the current study was able to characterise specific characteristics of mind wandering and self-control that may benefit from increasing the provision of glucose to the brain. Selfcontrolled attention (Galliot and Baumeister 2009) consumes a large amount of energy within the brain, and because glucose stores in the brain are limited (Mark and Rose 1981), consuming a glucose-containing drink can redress the balance. It is clear from the present study findings that glucose is effective at maintaining an individual’s focus on the task at hand and at buffering “fear of failure” related thoughts which may distract them from efficient task processing.

Acknowledgments We would like to thank Dr. Michael Smith and the reviewers for the very helpful comments on the final draft of the paper. We would like to also thank Dr. Debbie Riby for the contributions on an early draft of the paper.

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