Cognitive fatigue and cortical-striatal network in old age

Abstract

Cognitive fatigue (CF) is among the most common and disturbing aging symptoms, and substantially interferes with activities demanding sustained mental effort. Here we examined the relationship between the cortical-striatal network and CF (assessed by the 18-item visual analogue scale) when a group of cognitively and physically healthy older adults participated in a 30-minute cognitively fatiguing task-related fMRI experiment. We also explored whether CF would interfere with the "Posterior-Anterior Shifting in Aging" (PASA) phenomenon, an aging-associated neural reliance on frontal regions to support cognitive capacity. We revealed that decreased connectivity strength of the cortical-striatal network over the course of the task was related to higher CF. Correlation between CF and the cortical-striatal network was more robust in anterior relative to posterior components. Moreover, a positive relationship between reliance on the anterior part of the cortical-striatal network and cognitive performance only existed among older adults experiencing low CF. These findings suggest a crucial role of the cortical-striatal network, especially the anterior component, in linking to CF. The PASA phenomenon may only be applicable to older adults without vulnerability to CF.

Keywords: Posterior-Anterior Shifting in Aging; cognitive fatigue; functional MRI; functional connectivity; striatum.

Figure 1

Cognitively demanding tasks used to induce CF. (A) The experimental paradigm included two cognitively fatiguing tasks during fMRI scanning, in a random order, across subjects. (B) Dual-1 back task was a letter-location task. (C) The Color-word Stroop task consisted of congruent and incongruent conditions on color.

Figure 2

CF profile for the entire sample. (A) The distribution of CF change (post-pre) induced by cognitive tasks during fMRI scanning. According to different perceived fatigue, two groups were selected: low-CF subgroup (12 subjects with CF change ≤ 0, shown in blue) and high-CF subgroup (14 subjects with CF change ≥ 1, shown in red). In addition, there were 20 subjects outside the high- or low-CF subgroups (shown in grey). (B) The VAS fatigue score before and after performing cognitive tasks for each group, showing significant difference between high- and low-CF subgroup. (C) The IIVRT in Block1 and Block6 for each group showed the performance change with time by CF subgroups. There were significant different trends in IIVRT change between high- and low-CF subgroup. (D) Higher CF was significantly associated with larger IIVRT change (worse cognitive performance). Note: CF, cognitive fatigue; IIVRT, intra-individual variability of reaction time. low-CF subgroup: blue; high-CF subgroup: red; others: gray.

Figure 3

The interaction effects of CF subgroup and task block on left and right cortical-striatal network connectivity. For the left cortical-striatal network, there were significant differences of connectivity change in L SFG, R ACC, L PCC and R Cuneus. For the right cortical-striatal network, there were significant differences of connectivity change in L MFG, L MFG2, L MedFG and L OG. During the fatiguing tasks, the connectivity strength of cortical-striatal network increased in low-CF group, while deceased in high-CF group. Note: L, left; R, right; SFG, superior frontal gyrus; ACC, anterior cingulate cortex; PCC, posterior cingulate cortex; MedFG, medial frontal gyrus, MFG, middle frontal gyrus; OG, occipital gyrus. CF, cognitive fatigue.

Figure 4

Correlations between connectivity change and CF in the entire sample. In the cortical-striatal network, the partial correlation analysis showed CF change was significantly correlated with the anterior regions, including L SFG, R ACC, L MFG, LMFG2 and L MedFG. The CF change showed negative correlation trend with the posterior regions but not significant, including L PCC, R Cuneus and L OG. Note: L, left; R, right; SFG, superior frontal gyrus; ACC, anterior cingulate cortex; PCC, posterior cingulate cortex; MedFG, medial frontal gyrus, MFG, middle frontal gyrus; OG, occipital gyrus. p values here are FDR-corrected across all regions. CF, cognitive fatigue; IIVRT, intra-individual variability of reaction time.

Figure 5

Relationships between the anterior and posterior cortical-striatal network functional connectivity and CF. (A) During the cognitively fatiguing tasks, both of the anterior and posterior network showed significant interaction effects between subgroup (high- vs. low-CF) and block (1 vs. 6), that connectivity strength increased in low-CF group while decreased in high-CF group (B) Although CF was negatively associated with change of anterior or posterior connectivity, the negative relationship was more robust in anterior cortical-striatal network. Note: CF, cognitive fatigue; IIVRT, intra-individual variability of reaction time.

Figure 6

Moderation analysis of relationship between PAS and cognitive function. There was a significant interacting effect between CF and PAS in predicting task performance, showing greater PAS was related to better cognitive performance (smaller IIVRT) in the low-CF subgroup while worse cognitive performance (larger IIVRT) in the high-CF subgroup. Consistently, CF also significantly interacted with PAS in predicting executive function. Note: CF, cognitive fatigue; IIVRT, intra-individual variability of reaction time. PAS, posterior-anterior shifting.