Stress and prospective memory: What is the role of cortisol?

https://doi.org/10.1016/j.nlm.2019.04.010Get rights and content

Highlights

  • Oral intake of cortisol does not affect focal and nonfocal prospective memory tasks.

  • This was observed independently of the influence of SNS and cognitive reappraisal.

  • Cortisol changes thus do not underlie potential stress effects on prospective memory.

  • Exploratory results suggest a circadian variation of prospective memory performance.

Abstract

Studies investigating effects of acute stress on Prospective Memory (PM) so far yielded heterogeneous findings. Although results were commonly attributed to stress-induced changes in cortisol, past research did not disentangle effects of cortisol from the effects of sympathetic nervous system (SNS) activation and cognitive reappraisal. The present study therefore aimed at investigating the mere effect of cortisol on PM tasks that differently involve prefrontal brain regions (nonfocal vs. focal PM tasks) via a placebo-controlled oral pharmacological intake of 10 mg hydrocortisone mimicking physiological responses to stress. Contrary to our prediction, enhanced levels of cortisol did not affect PM accuracy and monitoring costs, neither for the focal nor the nonfocal PM tasks. These results suggest that changes of cortisol levels do not underlie potential stress effects on PM. Further exploratory results revealed that PM performance was higher in the 3 pm than in the 1 pm placebo group. This means that PM performance, independently of effects of cortisol, seem to vary throughout the day.

Introduction

Imagine you need to remember to pass by the bakery on your way home from work to buy bread. This task involves remembering to carry out an intended action at an appropriate point in the future while being engaged in an ongoing activity. This memory for an intention is defined as prospective memory (PM; McDaniel & Einstein, 2007), an ability of great importance for our quality of life (Hering et al., 2018, Woods et al., 2015), as it is highly relevant for our daily activities (e.g., remembering to take the cake out of the oven after 30 min), our health (e.g., remembering to take medication according to a certain schedule), and for maintaining independence (e.g., remembering to buy food). Despite the high importance of PM, its functioning under certain environmental contexts remains unclear. One of these conditions is stress, which is pervasively present in daily life. Returning to the example of remembering to buy bread on the way home from work, how would performance on that task change when you were just fired from your job?

So far, only a few studies have investigated the impact of stress on PM yielding heterogeneous findings (for review, see Piefke & Glienke, 2017). While some studies did not show any impact of stress on PM performance (Ihle et al., 2014, Möschl et al., 2017, Nater et al., 2006, Szollosi et al., 2018, Walser et al., 2013, for event-based PM), others demonstrated stressed vs. control participants to show enhanced PM performance (Glienke and Piefke, 2016, Nater et al., 2006, for time-based PM) or stress-induced PM impairment (Ihle, Schnitzspahn, Rendell, Luong, & Kliegel, 2012, assessing PM in a naturalistic environment).

Besides using different PM tasks, one key reason for these incoherent results might lie in variability in the physiological changes and subjective evaluation that the different employed stressors evoked, i.e., naturally occurring everyday stress (Ihle et al., 2012) versus laboratory stressors like the Trier Social Stress Test (TSST; Nater et al., 2006, Walser et al., 2013) or the Socially Evaluated Cold Pressor-Test (SECPT; Glienke and Piefke, 2016, Szollosi et al., 2018). This variation makes it difficult to characterize the underlying mechanisms of acute stress effects on PM.

Given that pharmacological administration of cortisol was shown to affect executive functions (Shields, Bonner, & Moons, 2015) as well as memory (Het, Ramlow, & Wolf, 2005), which both are closely related to PM (Zuber, Kliegel, & Ihle, 2016), studies commonly attributed stress effects on PM to the enhanced levels of cortisol following stress induction. Indeed, Glienke and Piefke (2017) reanalyzed data of their 2016 study of stress-induced cortisol changes and compared high and low cortisol responders, demonstrating that low responders’ PM performance benefitted from stress exposure, whereas high responders’ PM potentially was impaired by stress.

However, in response to a stressful event, the body naturally not only releases the stress hormone cortisol via the activation of the hypothalamus-pituitary-adrenal (HPA) axis, it also rapidly releases the stress hormones adrenaline/noradrenaline via an activation of the sympathetic nervous system (SNS) (Biondi and Picardi, 1999, Dickerson and Kemeny, 2004, Kirschbaum et al., 1993, Miller and O'Callaghan, 2002). Common stress inductions as the TSST and the SECPT consequently affect both the HPA axis and the SNS and thus stress effects on PM cannot be solely attributed to enhanced levels of cortisol, but might also root in changes in SNS activation.

Moreover, studies using experimental stress induction mostly investigated PM a certain time after the stress induction took place. At that moment, cortisol levels are indeed at their peak, but cognitive evaluation processes including coping strategies have equally started, resulting in a situation in which the stress-related effects of cortisol are confounded with cognitive post-stress appraisal (Gaab, Rohleder, Nater, & Ehlert, 2005). All in all, although present studies explain PM effects by enhanced stress-induced cortisol, it is yet unclear whether increased cortisol levels directly affect PM performance, in particular in isolation from alternative effects of stress mechanisms, such as autonomic SNS activation and cognitive reappraisal mechanisms also triggered by stress. Hence, the first aim of the present study was to experimentally test the mere effect of cortisol on PM performance by using a placebo-controlled pharmacological administration design.

Additionally, a wide variety of different PM task has been used in previous research that differ in how much strategic monitoring capacity is required to detect the PM target cue within the ongoing activity. In so-called focal PM tasks, spontaneous retrieval is sufficient to detect the target cue, as it is already processed in the course of the ongoing task. This is not the case in nonfocal PM tasks, which require a larger amount of strategic frontal capacity to monitor the occurrence of the target cue (i.e., controlled PM processing, see Einstein et al., 2005). Consequently, performance in nonfocal PM tasks is often lower than in focal tasks. Importantly, nonfocal tasks rely to a stronger extend on prefrontal regions than focal tasks (Cona et al., 2016, McDaniel et al., 2013, McDaniel et al., 2015). As cortisol was shown to affect the prefrontal cortex (Arnsten, 2009), it seems reasonable to expect that nonfocal tasks will be more strongly affected by cortisol. The second aim of the study was thus to investigate whether cortisol differently affects focal vs. nonfocal PM tasks. Given the underlying neural substrates of these tasks, it was predicted that nonfocal tasks are more strongly affected by cortisol, as these tasks rely on prefrontal processing. Only one study so far compared the effects of acute TSST-induced stress on nonfocal and focal tasks, reporting that both focal and nonfocal PM performance was unaffected by acute stress, but that ongoing task costs were reduced in the stress compared to the control group in the nonfocal, but not in the focal condition (Möschl et al., 2017).1 Further investigation of stress effects, particularly of cortisol effects, on focal compared to nonfocal tasks is thus strongly required.

In sum, the first goal of the present study was to investigate how cortisol affects PM performance by administration of 10 mg cortisol vs. placebo. This dose of cortisol mimics the physiological responses to stress, but crucially does not affect SNS activity (Schwabe, Oitzl, Richter, & Schächinger, 2009) and internal states that make participants aware of treatment (van Ast, Cornelisse, Meeter, Joels, & Kindt, 2013). Our second aim was to examine whether potential cortisol effects vary with regard to how strongly the PM task relies on prefrontal areas.

Section snippets

Participants

Fifty-seven right-handed participants aged 19–30 years (M = 22.25, SD = 2.29) took part in the study. Concerning education level, all participants were students of the University of Geneva that held a high-school diploma as university entry requirement. As such, average education level did not differ between the group assigned placebo and the group assigned cortisol. Participants had to be non-smokers (less than 10 cigarettes/day) and women had to be on hormonal contraception to avoid

Cortisol levels

Changes of cortisol levels across time is displayed in Fig. 1. A 2 (group: cortisol, placebo) × 7 (time: t0, t1, t2, … , t6) mixed-factorial ANOVA on cortisol levels demonstrated a significant main effect of group, F(1, 49) = 22.73, p < .01, ηp2 = 0.32, of time, F(2.25, 110.03) = 7.19, p < .01, ηp2 = 0.13, as well as an interaction of group × time, F(2.25, 110.03) = 11.54, p < .01, ηp2 = 0.19. Post hoc planned comparisons showed significant higher cortisol levels in the cortisol group compared

Discussion

The present study set out to (1) investigate isolated effects of the stress hormone cortisol on PM and to (2) examine whether these effects would differ between focal and nonfocal PM tasks that should differently involve the prefrontal cortex due to their monitoring demands. Manipulation checks revealed that pharmacological administration of hydrocortisone vs. the placebo clearly enhanced salivary cortisol levels, but did not affect salivary alpha-amylase levels, suggesting that activity of the

Acknowledgements

NB, MK and UR belong to the Swiss National Center of Competences in Research LIVES – Overcoming vulnerability: life course perspectives, which is financed by the Swiss National Science Foundation (grant number: 51NF40-160590). The authors are grateful to the Swiss National Science Foundation for its financial assistance. UR further acknowledges support by the Pierre Mercier Foundation.

Declarations of interest

None.

References (42)

  • G.S. Shields et al.

    The effects of acute stress on core executive functions: A meta-analysis and comparison with cortisol

    Neuroscience & Biobehavioral Reviews

    (2016)
  • A. Szollosi et al.

    Acute stress affects prospective memory functions via associative memory processes

    Acta Psychologica (Amst)

    (2018)
  • V.A. van Ast et al.

    Time-dependent effects of cortisol on the contextualization of emotional memories

    Biological Psychiatry

    (2013)
  • A.F.T. Arnsten

    Stress signalling pathways that impair prefrontal cortex structure and function

    Nature Reviews Neuroscience

    (2009)
  • N. Ballhausen et al.

    The interplay of intention maintenance and cue monitoring in younger and older adults' prospective memory

    Memory & Cognition

    (2017)
  • M. Biondi et al.

    Psychological stress and neuroendocrine function in humans: The last two decades of research

    Psychotherapy and Psychosomatics

    (1999)
  • G. Cona et al.

    Effects of cue focality on the neural mechanisms of prospective memory: A meta-analysis of neuroimaging studies

    Scientific Reports

    (2016)
  • S.S. Dickerson et al.

    Acute stressors and cortisol responses: A theoretical integration and synthesis of laboratory research

    Psychological Bulletin

    (2004)
  • G.O. Einstein et al.

    Multiple processes in prospective memory retrieval: Factors determining monitoring versus spontaneous retrieval

    Journal of Experimental Psychology-General

    (2005)
  • K. Glienke et al.

    Stress-related cortisol responsivity modulates prospective memory

    Journal of Neuroendocrinology

    (2017)
  • A. Hering et al.

    Prospective memory is a key predictor of functional independence in older adults

    Journal of the International Neuropsychological Society

    (2018)
  • View full text