Hyperthermia-Induced Disruption of Functional Connectivity in the Human Brain Network

Abstract

BackgroundPassive hyperthermia is a potential risk factor to human cognitive performance and work behavior in many extreme work environments. Previous studies have demonstrated significant effects of passive hyperthermia on human cognitive performance and work behavior. However, there is a lack of a clear understanding of the exact affected brain regions and inter-regional connectivities.Methodology and Principal FindingsWe simulated 1 hour environmental heat exposure to thirty-six participants under two environmental temperature conditions (25°C and 50°C), and collected resting-state functional brain activity. The functional connectivities with a preselected region of interest (ROI) in the posterior cingulate cortex and precuneus (PCC/PCu), furthermore, inter-regional connectivities throughout the entire brain using a prior Anatomical Automatic Labeling (AAL) atlas were calculated. We identified decreased correlations of a set of regions with the PCC/PCu, including the medial orbitofrontal cortex (mOFC) and bilateral medial temporal cortex, as well as increased correlations with the partial orbitofrontal cortex particularly in the bilateral orbital superior frontal gyrus. Compared with the normal control (NC) group, the hyperthermia (HT) group showed 65 disturbed functional connectivities with 50 of them being decreased and 15 of them being increased. While the decreased correlations mainly involved with the mOFC, temporal lobe and occipital lobe, increased correlations were mainly located within the limbic system. In consideration of physiological system changes, we explored the correlations of the number of significantly altered inter-regional connectivities with differential rectal temperatures and weight loss, but failed to obtain significant correlations. More importantly, during the attention network test (ANT) we found that the number of significantly altered functional connectivities was positively correlated with an increase in executive control reaction time.Conclusions/SignificanceWe first identified the hyperthermia-induced altered functional connectivity patterns. The changes in the functional connectivity network might be a possible explanation for the cognitive performance and work behavior alteration.

Cognitive and perceptual responses during passive heat stress in younger and older adults

“…The ability to perceive warm and cool temperatures is generally reduced with age (66). Furthermore, a given reduction in internal temperature elicits less thermal discomfort in older, compared with younger, adults (21).…”

“…This chronological cognitive decline may contribute to the risk of deleterious outcomes during heat waves in older adults by, for instance, leading to poor decision-making. Interestingly, perhaps because of the deleterious impact of heat stress on cerebral blood flow (46,61) and/or disruptions in cerebral functional connectivity (66), many cognitive processes are impaired in heat-stressed younger adults [e.g., aspects of attention (19,22,65), memory (6,19,28,41,54), and executive function (16,17,67)], although this is not always observed (3,50,61). If heat stress-induced impairments in cognitive function are amplified with age, this might suggest that the contribution of cognitive factors to the risk of morbidity and mortality during heat waves would be exacerbated in older adults.…”

Environmental heat exposure and cognitive performance in older adults: a controlled trial

“…Most studies investigating the effects of thermal stress on cognitive performance have recruited young adults to ascertain how heat stress may affect abilities that are crucial for military personnel (Radakovic et al 2007;Hocking et al 2001) and industry workers exposed to extreme environments (Sun et al 2013;Simmons et al 2008;Gaoua 2010). However, to the best of our knowledge, no studies have directly investigated the effects of hot environments on the cognitive functioning of older adults.…”

Phenotypic and Genetic Correlations Between the Lobar Segments of the Inferior Fronto-occipital Fasciculus and Attention

“…In patients with multiple sclerosis, better cognitive performance was correlated with increased functional connectivity between anterior cingulate cortex and occipital lobe46. Moreover, the decreased functional connectivity between the anterior cingulate cortex and occipital lobe was associated with the increase in executive reaction time47.…”