Elsevier

Neuroscience Research

Volume 146, September 2019, Pages 48-53
Neuroscience Research

Performance fatigability does not impact the inhibitory control

https://doi.org/10.1016/j.neures.2018.10.002Get rights and content

Highlights

  • We tested whether performance fatigability of finger flexor muscles affects the inhibitory control.

  • A significant strength reduction in response effectors was found.

  • The effectors-related muscle fatigability does not impair inhibitory processes.

Abstract

This study explored whether reduction of the maximal voluntary force of finger flexor muscles affects response inhibition processing while performing the flanker “inhibitory reaction time” task. Sixteen participants completed two experimental sessions: each consisted of either a fatiguing exercise (fatigue session) or a control task (control session) followed by a flanker task. When responding to 32 compatible and 32 incompatible trials, the participants were asked to respond to a right-facing arrow by pressing a button beneath their middle finger, and to a left-facing arrow by pressing a button beneath their index finger. During the fatigue session, the participants were instructed to sustain 50% of their maximal voluntary isometric force during a handgrip force task with their wrist in a neutral position. In the control session, this exercise was replaced by a 7-min period of rest. The results showed that the handgrip task was effective at inducing a significant decrease in maximal force (-25.2 ± 9.1%, p < 0.001). However, this performance fatigability did not affect either the reaction time or the error rate. Similarly, it did not alter the conflict-monitoring function involved in the settings of response override. A functional robustness of the inhibition function under fatigue effect is assumed, at least in young healthy adults.

Introduction

Cognitive control refers to a suite of cognitive processes that enable individuals to adapt to challenging environment in a goal-directed manner (Groom and Cragg, 2015). Amongst those processes, the ability to inhibit an automatic, prepotent or even inappropriate response is crucial. It allows flexible, adaptive and complex goal-directed responses in changing environments (Diamond, 2013). For instance, the inhibition capacities constitute one reliable predictor for achieving expertise in ball sports (Vestberg et al., 2012).

In this context, it is well evidence-based that « fatigue » associated with repetitive motor tasks or exercise leads to deterioration of cognitive functions and consequently, of performance. Several studies have supported that fatigue affects high-level cognitive processes (Lorist et al., 2002). For example, some works showed that localized muscle fatigue increased the attentional cost associated with the maintenance of efficient motor performance (Forestier and Nougier, 1998; Vuillerme et al., 2002). In a visual search flanker/response competition task, other evidence showed that (i) participants having the worst reaction time (RT) performances had the lowest baseline physical fitness, and (ii) their RT increased when they were engaged in an hour-long bout of pedaling exercise, indicating impairment in selective attention (Bullock and Giesbrecht, 2014). Overall, numerous studies showed a small but beneficial effect of a single bout of aerobic or resistance exercise on cognitive performance and executive control, irrespective of age (see Chang et al., 2012 or McMorris and Hale, 2012, for a meta-analyses).

It is unknown whether an acute exercise-induced reduction in force, referred to herein as performance fatigability (Enoka and Duchateau, 2016) affects inhibitory control. This gap in knowledge could be partly explained by the complexity of inducing fatigue in laboratory conditions that is comparable to fatigue encountered in a natural context (Lambourne and Tomporowski, 2010). The definition of fatigue is intricate, requiring the need to go beyond its classical central-peripheral dichotomy (Enoka and Duchateau, 2016). Here, we considered performance fatigability as an acute exercise-induced reduction in force and power output of the muscles involved in performance, which was quantified by a reduction of maximal voluntary contraction (Enoka and Duchateau, 2016).

To address this issue, we used the Eriksen flanker interference task (Eriksen and Eriksen, 1974), in which the participants are instructed to respond as quickly as possible by button-press by considering the central stimulus (“<” or “>”) and ignoring 4 flanking stimuli pointing in the same direction (< < < < < or > > > > > compatible trials) or in the opposite direction (> >< > > or < < >< < incompatible trials). Studies have consistently reported the longest RTs in incompatible trials. This so-called flanker effect has been investigated in studies that addressed the impact of non-fatiguing exercise while performing an RT task (Davranche et al., 2015). These works showed a significant facilitatory effect, or at least no adverse effect, on cognitive control (Chang et al., 2012). To the best of our knowledge, only one study has tested the effect of overall physical fatigue on cognitive inhibition (Schmit et al., 2015). Participants had to perform a flanker task while completing an arduous cycling bout, until exhaustion. Even if RT was not impacted, participants tended to commit more errors in the incompatible condition while pedalling. But the effects of performance fatigability on inhibitory processes engaged during the performance remain to be explored, in particular with respect to the conflict-monitoring and selection-for-action processes (Botvinick et al., 1999).

Studies of the anterior cingulate cortex (ACC), which is engaged in response to a conflict situation, have validated the dissociation between a function that monitors and detects conflicts in information processing (e.g. in tasks requiring the overriding of inappropriate prepotent response) and a top-down attentional control mechanism required for selecting the appropriate response (Botvinick et al., 2001, Botvinick et al., 2004). Practically, this dissociation can be evaluated by analyzing the compatibility of the preceding trial in the flanker task. Indeed, the RT from an incompatible trial is shorter if preceded by an incompatible trial (iI condition, i.e. high control with low conflict), a facilitation effect known as the Gratton effect. However, the incompatible RT increases when it follows a compatible trial (cI condition, i.e. low control with high conflict). The Gratton effect results from a cognitive conflict reduction, leading to a strengthening of selection-for-action.

The conflict-monitoring theory, and more broadly, the recent integrative model of expected value of control (Shenhav et al., 2013), postulates the role of the ACC to increase attentional resources in tasks where one response has to be selected among conflicting ones. A series of neuroimaging studies validated the core role of the ACC in implementing the conflict-detection monitoring mechanism (Botvinick et al., 1999; Botvinick, 2007; Braver et al., 2001; Lee et al., 2001; Ruff et al., 2001), evidenced by its strongest engagement in actual response to the cI flanker trials (Botvinick et al., 1999; MacDonald et al., 2000). All of this is consistent with studies showing impairments in Stroop conflict performance in patients with ACC lesions, but only when manual responses are involved (Turken and Swick, 1999). In brief, the ACC seems to be critical for monitoring the presence of response conflict (Paus et al., 1993; Van Veen et al., 2001). Interestingly, this specific ACC activation was located in the rostral cingulate motor zone, in accordance with the maximum activation seen in the ACC confluent with the supplementary motor area during a choice reaction task (Winterer et al., 2002). Note also that the ACC communicates with the dorsolateral prefrontal cortex and parietal cortex to account for conflict-monitoring (Carter et al., 2000).

The expected changes in brain activation of motor areas subsequent to a fatiguing motor task are also associated with activation in a number of association cortices, such as the prefrontal cortex, parietal cortex and cingula (BA 24, 31) (Dai et al., 2001; Korotkov et al., 2005). As performance fatigability occurs, functional activation of the prefrontal cortex and cingula (BA24 in particular) likely reflects the concomitant attentional control for task performance maintenance (Winterer et al., 1996). Moreover, ACC is assumed to be functionally linked to motor areas and behaves as a mediator of the central command (Carson and Kelso, 2004). Direct connections between the ACC and motor areas as well as the level of the spinal cord (see Dum and Strick, 2002) suggest strong functional regulation during the preparation and generation of movement sequences (Shima and Tanji, 1998). Finally, the supraspinal model to regulate physical fatigue (Tanaka and Watanabe, 2012) suggests that the ACC is sending both facilitatory and inhibitory information to motor areas. As such, the performance fatigability-related afferences might modulate ACC activation and makes the implementation of the conflict-detection monitoring mechanism more difficult and less automatic.

These similar patterns of brain activation for inhibitory control and acute fatigue suggest that both functions share neural networks, through functional connections between ACC and motor corticospinal pathways. Within this context, fatigue-related changes in internal states should impact the response conflict monitoring. Hence, we aimed to determine whether a reduction in the force-generating capacity of muscles involved in the flanker task alters inhibitory control. The inhibitory reaction time performance in the flanker task was assessed during two experimental sessions: a handgrip fatiguing session and a control resting session. Considering the potential interference from engagement of similar neural networks underlying the processes of both muscle fatigue and inhibitory requirements, we hypothesized that performance fatigability would alter the response conflict-monitoring process, evidenced by longer reaction time and smaller response accuracy in incompatible trials. Moreover, because of the specific contribution of the ACC to the detection of conflicts, we expected longer RT for the most conflicting condition as compared to the less conflicting one.

Section snippets

Participants

Sixteen healthy right-handed male volunteers (mean age 20.8 ± 1.2 years), presenting no motor or perceptual deficits, participated in this experiment. They had no previous experience with the flanker task, and were informed clearly of the purpose of the study before providing written consent. This study was conducted in accordance with the Helsinki statement.

General procedure

Participants completed two experimental sessions that were separated by at least two days. Each consisted of either a fatiguing exercise

MVCs

There was a significant effect of both Session [F(1,14) = 39.3, p < 0.001, ηp2 = 0.74, BF01 = 0.0001] and Time [F(4,56) = 41.3, p < 0.001, ηp2 = 0.75, BF01 < 0.00001] on the index finger MVC. Similar results were obtained for the middle finger with a significant effect of Session [F(1,14) = 15.9, p < 0.01, ηp2 = 0.53, BF01 = 0.013] and Time [F(4,56) = 37.5, p < 0.001, ηp2 = 0.73, BF01 < 0.00001]. In addition, a Session × Time interaction was found for both fingers [index: F(4, 56) = 11.7, p <

Discussion

The aim of this study was to explore the impact of performance fatigability on cognitive inhibition during the Eriksen flanker task. Contrary to our hypothesis, there was no effect of fatigability on incompatible RTs (i.e. trials requiring the overriding of prepotent response) and response accuracy.

The first results to consider are those obtained during the fatigue session, where the fatigue of muscles involved in the RT task was induced experimentally by a prolonged intermittent submaximal

Conclusion

In summary, the present findings show that the force loss induced in the response effectors used in the flanker RT task did not affect inhibitory control. No change in RT and accuracy performance was observed in the incompatible trials; a functional robustness of the inhibition function under fatigue effect can be assumed, at least in young healthy adults. Future studies should aim to further investigate if performance fatigability does not affect cognitive inhibition, in particular by using

Conflict of interest

The authors report no conflicts of interest.

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