Low putamen activity associated with poor reward sensitivity in childhood chronic fatigue syndrome

Abstract

Motivational signals influence a wide variety of cognitive processes and components of behavioral performance. Cognitive dysfunction in patients with childhood chronic fatigue syndrome (CCFS) may be closely associated with a low motivation to learn induced by impaired neural reward processing. However, the extent to which reward processing is impaired in CCFS patients is unclear. The aim of the present functional magnetic resonance imaging (fMRI) study was to determine whether brain activity in regions related to reward sensitivity is impaired in CCFS patients. fMRI data were collected from 13 CCFS patients (mean age, 13.6 ± 1.0 years) and 13 healthy children and adolescents (HCA) (mean age, 13.7 ± 1.3 years) performing a monetary reward task. Neural activity in high- and low-monetary-reward conditions was compared between CCFS and HCA groups. Severity of fatigue and the reward obtained from learning in daily life were evaluated by questionnaires. Activity of the putamen was lower in the CCFS group than in the HCA group in the low-reward condition, but not in the high-reward condition. Activity of the putamen in the low-reward condition in CCFS patients was negatively and positively correlated with severity of fatigue and the reward from learning in daily life, respectively. We previously revealed that motivation to learn was correlated with striatal activity, particularly the neural activity in the putamen. This suggests that in CCFS patients low putamen activity, associated with altered dopaminergic function, decreases reward sensitivity and lowers motivation to learn.

Neurostructural correlates of optimism: Gray matter density in the putamen predicts dispositional optimism in late adolescence

“…Therefore, we surmised that the finding of the putamen, whose rGMD was linked to dispositional optimism, may reflect the motivational characteristics of dispositional optimism. More concretely, the putamen has been demonstrated to be involved in several motivation‐related processes, for example, history‐based reward value encoding, action selection, and cue‐action‐dependent reward prediction (Elliott, Newman, Longe, & Deakin, ; Haruno & Kawato, ; Hori, Minamimoto, & Kimura, ; Kunimatsu, Maeda, & Hikosaka, ; Mizuno et al, ; Muranishi et al, ; Pessiglione, Seymour, Flandin, Dolan, & Frith, ; Schultz, ). For example, several studies have shown that the putamen was closely associated with reward value encoding and action selection based on past experience (Kunimatsu et al, ; Muranishi et al, ), and that these processes, i.e., history‐based reward value updating and action selection, were impaired if the neural activity in the putamen was blocked (Muranishi et al, ).…”

“…More concretely, the putamen has been demonstrated to be involved in several motivation-related processes, for example, history-based reward value encoding, action selection, and cue-action-dependent reward prediction (Elliott, Newman, Longe, & Deakin, 2004;Haruno & Kawato, 2006;Hori, Minamimoto, & Kimura, 2009;Kunimatsu, Maeda, & Hikosaka, 2019;Mizuno et al, 2016;Muranishi et al, 2011;Pessiglione, Seymour, Flandin, Dolan, & Frith, 2006;Schultz, 2000).…”

Changes in fatigue, autonomic functions, and blood biomarkers due to sitting isometric yoga in patients with chronic fatigue syndrome

“…This result suggests that dopaminergic activation may be related to the yoga-induced increase in vigor. Previous studies have demonstrated that patients with CFS exhibited reduced neural activation of the caudate nucleus in response to a reward task [ 16 ] and of the putamen [ 17 ], which may be due, in part, to dopaminergic dysfunction [ 16 , 17 ]. Thus, reduced dopamine activity may contribute to symptoms of low energy in patients with CFS and dopaminergic activation may have a beneficial effect.…”

“…Dysfunctions of the immune system include increased blood levels of multiple cytokines, including transforming growth factor (TGF)-β1 and several proinflammatory cytokines such as tumor necrosis factor (TNF)-α, interleukin (IL)-6, and interferon (IFN)-γ [ 12 – 15 ]. Dysfunctions of the CNS include hypoactivity of the dopaminergic nervous system to reward stimuli [ 16 , 17 ]. Other dysfunctions in patients with CFS include lower blood levels of acylcarnitine than in healthy subjects [ 18 , 19 ].…”

Altered right anterior insular connectivity and loss of associated functions in adolescent chronic fatigue syndrome

“…Decreases in motivational neural circuitry were associated with increases in mental and general fatigue and reductions in physical activity in adult CFS [ 81 ]. Previous fMRI studies with children and adolescents with CFS found changes in activities of the prefrontal and parietal regions during attentional control [ 82 ] and decreases in striatal activity involved in reward sensitivity and motivation [ 83 ].…”