Research report
Impaired cognitive control and reduced cingulate activity during mental fatigue

https://doi.org/10.1016/j.cogbrainres.2005.01.018Get rights and content

Abstract

Neurocognitive mechanisms underlying the effects of mental fatigue are poorly understood. Here, we examined whether error-related brain activity, indexing performance monitoring by the anterior cingulate cortex (ACC), and strategic behavioural adjustments were modulated by mental fatigue, as induced by 2 h of continuous demanding cognitive task performance. Findings that (1) mental fatigue is associated with compromised performance monitoring and inadequate performance adjustments after errors, (2) monitoring functions of ACC and striatum rely on dopaminergic inputs from the midbrain, and (3) patients with striatal dopamine deficiencies show symptomatic mental fatigue, suggest that mental fatigue results from a failure to maintain adequate levels of dopaminergic transmission to the striatum and the ACC, resulting in impaired cognitive control.

Introduction

Mental fatigue refers to the effects that people experience following and during the course of prolonged periods of demanding cognitive activity, requiring sustained mental efficiency. It is, at least to some extent, a common part of many daily-life activities, such as taking part in traffic, or operating complex computer programs or machinery. Mental fatigue may lead to sub-optimal functioning or even human error. In extreme cases, these failures give rise to catastrophic events such as traffic accidents or surgical imprecision. Despite these obvious perils, little is known about the cognitive processes affected by mental fatigue or the neurocognitive mechanisms underlying these effects [7], [19], [20].

Here, we examined the hypothesis that the effects of mental fatigue on neurocognitive function involve mechanisms of cognitive control. Cognitive control refers to those emergent ‘higher-order’ mental functions that oversee and regulate more basic cognitive functions in accordance with internal intentions [17], [24]. Theories of cognitive control suggest that these control mechanisms are implemented in the brain in a distributed network, involving closely interacting components that are engaged in monitoring and evaluating behaviour (overseeing) and in the implementation of executive control (regulation) when adjustments in control are needed [6], [22], [23]. The engagement of cognitive control is crucial especially under novel and complex task demands, conditions under which fatigued individuals most prominently experience performance difficulties.

Neuroimaging studies and event-related brain potential research have established that the ACC is central to performance monitoring [3], [13], [21], [34]. ACC is thought to detect the activation of erroneous or conflicting responses and to signal the need to activate adaptive control processes, serving to instigate remedial performance adjustments that minimise the risk of subsequent error [1], [6], [18]. Such interventions may involve immediate corrective actions (e.g., post-error slowing) or long-term strategic adjustments (e.g., tonic changes in speed/accuracy balance) [13], [28]. Neural activity in the ACC has been found to change with time-on-task [5], [26], suggesting that alterations in ACC functioning are a possible mechanism of mental fatigue. The monitoring function of ACC relies on the mesencephalic dopamine system [2], [16], which projects diffusely to the cortex and the striatum [16]. Disturbances in the striatal system have also been related to mental fatigue [4], supporting the dopaminergic involvement in mental fatigue. If prolonged periods of demanding cognitive activity result in reduced mesencephalic dopaminergic projections to ACC, the consequence may be impaired performance monitoring and inadequate performance adjustment.

An electrophysiological index of performance monitoring in ACC is the error-related negativity (ERN or Ne) [8], [14], which occurs immediately following the response. This event-related brain potential (ERP) is observed when subjects generate an error or when task conditions elicit high levels of response conflict [1], [3], [16], [21], [35]. Based on the association between ERN/Ne amplitude and the role of ACC in error monitoring, observed consistently in the literature [3], [13], [16], [21], [34], the ERN/Ne can be used to examine the effects of psychoactive substances, such as alcohol [30], or state variables, such as fatigue [9], [32] on cognitive control mechanisms. The ERN/Ne amplitude was observed to be reduced after sleep deprivation [32]. Consistent with observations that cognitive failures associated with sleep-deprivation can be counteracted by caffeine [36], ERN/Ne amplitude is increased after moderate doses of caffeine consumption [33].

The current investigation was designed to assess whether performance monitoring involving the ACC, as indexed in the ERN/Ne, and related post-error adjustments in behaviour, were modulated by mental fatigue, induced by 2 h of prolonged task performance. To this end, we examined ERPs in a study designed to track the effects of fatigue on error monitoring, as well as remedial behavioural adjustments subsequent to errors. Participants performed a variant of the Eriksen flanker task, in which they searched for a centrally presented target letter that was flanked by distracter stimuli, associated either with the same response as the target (compatible condition) or with the opposite response (incompatible condition). The subjects' task was to respond to the target letter and ignore distracting information. This task was selected because of its demonstrated success at eliciting ERNs/Nes [1], [16].

Section snippets

Participants

Fifteen healthy young women, ranging in age from 19 to 25 years (M = 21.1, SD = 1.8), participated in the study. All reported to be non-smokers, to have normal sleep patterns, not to work night shifts, and not to use prescription medication. They all had normal or corrected-to-normal visual acuity and were right-handed according to self-report. Subjects received a monetary bonus in return for their participation. Informed consent was obtained from all subjects prior to the study.

Stimuli and apparatus

Stimuli were

Results

Dependent variables were entered into univariate repeated-measures analysis of variance in SPSS, using the ɛ*-adjustment procedure recommended by Quintana and Maxwell [27]. For clarity, uncorrected df values are presented.

Discussion

Although performance detriments as a function of mental fatigue have been documented across a broad spectrum of cognitive tasks [7], [19], [20], the neurocognitive mechanisms underlying these effects have remained elusive. Building on the hypothesis that these effects involve mechanisms of cognitive control, we examined the effects of prolonged task performance on error processing. The present study documents that mental fatigue results in compromised error monitoring as reflected in a

Acknowledgments

This work was supported by grants from The Netherlands Organization for Scientific Research (M.M.L.; concerted research action “Fatigue at Work”) and the School of Behavioural and Cognitive Neurosciences (M.M.L.; Groningen, The Netherlands).

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