Nature as a potential modulator of the error-related negativity: A registered report

Highlights

• Attention Restoration Theory suggests that cognitive control abilities are improved when participants spend time in nature

• We examine whether or the ERN, a cognitive control component related to error-processing, will change as a result of nature exposure.

• We find an increase in ERN amplitude when people are in nature, which we suggest reflects restored cognitive control

Abstract

According to Kaplan's Theory of Attention Restoration (ART), spending time in a natural environment can restore depleted cognitive resources. If this is true, then nature exposure may modulate the error-related negativity (ERN), a component of the event-related brain potential (ERP) that is related to cognitive control and attentional allocation. ART suggests that cognitive resources are restored because the cognitive control networks of the brain are less engaged in nature, suggesting that the ERN may decrease in nature. In the present study, we completed a registered report, examining whether or not spending time in nature would reduce the size of the ERN compared to outdoor testing. Instead, we found that nature significantly increased the amplitude of the ERN. The implications of these results are discussed within the ART framework.

Introduction

In modern society, outside time is an increasingly rare commodity. Approximately ¼ of Americans spend less than 2 h a week outside, and another 1/3 spend only 5 h or less outside, despite reporting interests in nature (Kellert et al., 2017). Barriers to nature may be attributed to indoor obligations such as work or school, but even in leisure time, natural environments may be difficult to find. By 2050, over 70% of Americans are expected to live in a city (Heilig, 2012), making nature mostly inaccessible. These numbers are troubling because of the health implications; time spent indoors or on busy streets may be a hindrance to one's ability to exercise (Ford et al., 2005). However, in addition to physical health issues, we may also be missing out on cognitive benefits by spending too much time inside.

Towards the end of the 20th century, Stephen Kaplan (1995) suggested in his well-known Attention Restoration Theory (ART) that there are cognitive benefits to interacting with nature. Over the past 20–30 years, a growing body of scientific evidence has emerged in the wake of ART, echoing what philosophers and writers have claimed for years (e.g. Abbey, 1968; Williams, 1995). Researchers have documented several cognitive changes that occur after spending time in nature. An hour-long walk in the park, for example, produces greater improvement on the backward digit span task than an hour-long walk through the city (Berman et al., 2008). Participants also exhibited better creative reasoning skills after a backpacking trip compared to control (Atchley et al., 2012); recently, these results were replicated on a canoe camping trip in the Boundary Waters (Ferraro, 2015). Additionally, people who had been exposed to nature performed better on proofreading tasks compared to people who were not exposed to nature (Hartig et al., 2003). Students performed better on attention tasks (Tennessen and Cimprich, 1995) and working memory tasks (Taylor et al., 2002) when tested next to a view of nature compared to an urban view. Subjectively, people report lower levels of mental fatigue and increased restoration after viewing scenes of nature (Berto, 2005; Felsten, 2009; Herzog et al., 2003; Laumann et al., 2001), particularly when exposed to scenes containing water (Purcell et al., 2001).

Overall, there is a growing body of evidence that interacting with nature affords cognitive (for a review see Ohly et al., 2016) and physiological benefits, and improves mood (Gidlow et al., 2016). However, very little research has examined neurophysiological correlates behind the “nature effect”. One study found that participants who went for a walk in nature showed reduced activity in the subgenual prefrontal cortex, an area associated with depression, after the walk compared to those who walked in an urban area (Bratman et al., 2015). Another study found that participants who listened to nature sounds demonstrated more functional connectivity within the default mode network (DMN), which is negatively associated with the Attention Network (Buckner et al., 2008), compared to those who listened to urban sounds (Van Praag et al., 2017). As each of these studies involved neuroimaging, neither was able to examine brain activity while participants were actually engaged with real world nature. Hence, electroencephalography, a relatively more portable technique, may be useful for this purpose.

Researchers have been able to document some electrophysiological brain responses to nature (e.g. Aspinall et al., 2015; Ulrich, 1981). For example, Ulrich (1981) found reduced resting alpha power, suggesting changes in attention processes (van Dongen-Boomsma et al., 2010). Another study (Aspinall et al., 2015) found that participants experienced decreases in signals related to frustration when walking in nature compared to an urban environment, however, these signals were not reported within the canonical oscillatory bands or localized to any particular brain region, so the results are difficult to interpret. While this type of research provides a promising avenue to explore potential neural mechanisms of the nature effect, we are aware of no studies that have explored task-related neurophysiological changes in cognitive processing in natural environments. One particular area of interest to the present study is how activity involved in attentional processes may change in nature.

ART (Kaplan and Kaplan, 1989) suggests that nature provides an important break from voluntary, top-down attentional control to involuntary, bottom-up control that is less cognitively demanding. Importantly, this shift from voluntary to involuntary attention is hypothesized to restore depleted attentional resources. For decades, scientists have established that attention draws on limited resources (Wickens, 1991) and that high attentional demands induce a state of cognitive fatigue, that impairs performance on subsequent tasks (Cohen and Spacapan, 1978; Dang, 2018). Kaplan argues that nature can replenish depleted resources by giving the attentional system “a break.” The use of cognitive electrophysiology may help to examine this claim systematically.

The present study attempts to understand if nature affects the error-related negativity (ERN); a neural component associated with goal-maintenance and error monitoring. If these processes associated with cognitive control and attention are muted in nature, we should expect to see a decrease in the ERN when participants spend time outside in nature. The ERN is a negative deflection in the event-related brain potential (ERP) that occurs when a participant makes a response inconsistent with the task goal (an error). It peaks around 50 ms post-response (Falkenstein et al., 1990, Falkenstein et al., 1991; Gehring et al. 1993). A dominant theory of the functional significance of the ERN is the motivational significance theory, which suggests that an individual's motivation to avoid errors influences the amplitude of the ERN (Gehring et al., 1993; Hajcak and Foti, 2008). For example, the ERN increases (becomes more negative) when participants are rewarded for better performance (Hajcak et al., 2005). This theory also has the potential to account for the influence of pathological anxiety to increase the amplitude of the ERN (Endrass et al., 2008; Gehring et al., 2000; Hajcak et al., 2003), as anxious individuals are more aversive to errors. In essence, the more one wishes to avoid an error, the larger the amplitude of the ERN is. By contrast, if one either is unmotivated to perform well or lacks the required resources to perform well, the ERN will diminish in size. As one might expect, if someone is overly invested in goal maintenance (e.g. anxiety patients), this process of error-monitoring would likely recruit attentional resources.

Several modeling studies have localized the ERN to the ACC (Dehaene et al., 1994, Holroyd et al. 1998, Miltner et al. 2003) and converging fMRI evidence has shown increased blood flow to the ACC in response to errors (Hester et al. 2004). Importantly, the ACC is part of the executive attention network (AN) – a brain network that is activated in tasks requiring cognitive control, exertion, or self-regulation (Corbetta and Shulman, 2002; Banfield et al., 2004; Shackman et al., 2011). Error-monitoring and goal maintenance also require recruitment of the AN (Corbetta and Shulman, 2002; Dosenbach et al., 2008). As the ERN is likely a manifestation of AN activity, we hypothesize that fewer attentional resources will be devoted to error-monitoring with long-term immersion in nature and that a decrease in the ERN will be a manifestation of this process.

Nature is thought to restore the brain from a state of cognitive fatigue by replenishing attentional resources (Kaplan, 1995). If the executive attention network is downregulated during nature immersion, we predict that the amplitude of the ERN would be reduced. We tested this hypothesis by recording EEG while participants performed an Eriksen Flanker Task (Eriksen and Eriksen, 1974) in a within-subjects design (before, during, and after a 5-day nature excursion). A decrease in the ERN during the nature excursion will provide evidence that nature downregulates the activity of AN.