Compensatory effort parallels midbrain deactivation during mental fatigue: an fMRI study - PubMed (original) (raw)
Compensatory effort parallels midbrain deactivation during mental fatigue: an fMRI study
Seishu Nakagawa et al. PLoS One. 2013.
Abstract
Fatigue reflects the functioning of our physiological negative feedback system, which prevents us from overworking. When fatigued, however, we often try to suppress this system in an effort to compensate for the resulting deterioration in performance. Previous studies have suggested that the effect of fatigue on neurovascular demand may be influenced by this compensatory effort. The primary goal of the present study was to isolate the effect of compensatory effort on neurovascular demand. Healthy male volunteers participated in a series of visual and auditory divided attention tasks that steadily increased fatigue levels for 2 hours. Functional magnetic resonance imaging scans were performed during the first and last quarter of the study (Pre and Post sessions, respectively). Tasks with low and high attentional load (Low and High conditions, respectively) were administrated in alternating blocks. We assumed that compensatory effort would be greater under the High-attentional-load condition compared with the Low-load condition. The difference was assessed during the two sessions. The effect of compensatory effort on neurovascular demand was evaluated by examining the interaction between load (High vs. Low) and time (Pre vs. Post). Significant fatigue-induced deactivation (i.e., Pre>Post) was observed in the frontal, temporal, occipital, and parietal cortices, in the cerebellum, and in the midbrain in both the High and Low conditions. The interaction was significantly greater in the High than in the Low condition in the midbrain. Neither significant fatigue-induced activation (i.e., Pre<Post), nor its interaction with factor Load, was identified. The observed midbrain deactivation ([PreH - PostH]>[PreE- PostE]) may reflect suppression of the negative feedback system that normally triggers recuperative rest to maintain homeostasis.
Conflict of interest statement
Competing Interests: The authors have declared that no competing interests exist.
Figures
Figure 1. Divided attention task.
A schematic of the range of visual and auditory stimuli (A) and an example showing the first three visual and auditory stimuli in an ‘easy’ sequence (B). V and A stimuli were independently presented in pseudo-random order. The V and A stimuli were presented at pseudo-random timings with stimulus onset asynchrony (SOA) of 1000, 1500, or 2000 ms. The+represents an inter-V stimulus interval, during which the screen showed a centered cross to maintain resting eye fixation. Twelve visual and 12 auditory stimuli constituted a 19-s block. A ‘hard’ block followed each ‘easy’ block. A run consisted of six easy blocks and six hard blocks, with 12-s inter-block pauses. Four sets of three runs separated by 54 s were conducted (the middle two runs were consecutive) during the 2-hour study. Subjects were instructed to press a button after each target stimulus (a different button for visual and auditory responses.).
Figure 2. Behavioral data (n = 29).
The mean percent accuracy (A) and mean reaction times (B) in both Pre and Post sessions during functional MRI scanning are shown for the easy and hard conditions. Each line indicates the subjective task difficulty of the easy and hard tasks, which were analyzed using a two-way ANOVA for factors Load (Easy vs. Hard) and Time (Pre vs. Post) (C). Each bar graph indicates the means of the subjective feelings of fatigue, aversion, and sleepiness in both Pre and Post sessions, which were analyzed using paired _t_-tests (D). Error bars indicate standard errors. * p<0.05; ** p<0.001. E, Easy; H, Hard; n.s., no significance; Post, the last three runs again in the magnetic resonance imaging (MRI) scanner; Pre, the first three runs in the MRI scanner.
Figure 3. Deactivation related to fatigue and compensatory effort (n = 29).
All voxels were significant at a statistical threshold of p<0.05 for family wise error (FWE) corrected for multiple comparisons. Fatigue-induced deactivation in the H condition (i.e., PreH – PostH) (A), fatigue-induced deactivation in the E condition (i.e., PreE – PostE) (B), and deactivation reflecting the compensatory effort (i.e., [PreH – PostH] – [PreE – PostE]) (C). The activation profile of each area represents the parameter estimates in each condition. Errors bar represent the standard errors. The coordinates in the MNI standard space are indicated. E, Easy; H, Hard; Post, the last three runs again in the magnetic resonance imaging (MRI) scanner; Pre, the first three runs in the MRI scanner.
Figure 4. Individual analyses.
Deactivation in the midbrain reflecting compensatory effort (i.e., [Pre H – PostH] – [PreE – PostE]) was re-analyzed on an individual basis within the subject's native space, and each anatomical image was overlain on the mid-sagittal section. All voxels were significant at a statistical threshold of p<0.05, uncorrected.
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