To our knowledge, this is first study to explore the altered FC of thalamus subregions underlying impaired attention after SD. The decreased FCs between thalamus subregions and cerebral cortices were detected after acute SD. Importantly, we found the significant correlation between the change in attention performance and the altered FC, which indicated the neural mechanism underlying impaired attention after SD.
The ANT is applied to evaluate the orientating, alerting and executive components of attention performance. In this study, we found the significant lower alerting effect and higher executive effect after SD, which indicated declines in alerting and executive functions. It had been confirmed that the attention performance was impaired after acute SD (Ning et al., 2022). In line with our study, our previous study on shift work disorder, a form of chronic SD, also showed lower alerting effect and higher executive effect compared with healthy controls (Ning et al., 2021). Several studies on SD revealed the same results with us (Heaton et al., 2014; Riontino et al., 2022). Nevertheless, in contrast to our result, one previous study on 47 participants also revealed decreased orientating effect after SD (Whitney et al., 2017). The inconsistent result could be due to the high inter-subject variability after SD (Banks et al., 2007). The relatively small sample size might be also the cause of no significant decrease on orienting effect after SD in our study. Moreover, our study also showed the lower accuracy after SD, which furtherly demonstrated attention declines after SD.
The role of the thalamus in attention decline after acute SD has been well documented. One recent resting-state fMRI study revealed increased ALFF in the thalamus after 24h SD (Cai et al., 2021). Another study on acute SD indicated the increased effective connectivity from the thalamus to the nodes in the frontal–parietal attention network, which was significantly correlated with decreased lapses (Y. Chen et al., 2022).These findings demonstrate the important role of the thalamus in attentional maintenance after SD. Numerous studies had confirmed that the thalamus played a vital role in the sleep–wake pathway and involved in cognitive functions, such as attention, working memory(Gent et al., 2018; Krause et al., 2017). Our findings showed the altered FC in thalamus subregions involving ‘somatosensory’ thalamic seed, ‘motor’ thalamic seed and ‘occipital’ thalamic seed. The ‘somatosensory’ thalamic seed and motor’ thalamic seed selectively control the flow of sensory-motor information to the cerebral cortex during different states of the sleep-wake cycle and arousal, which are controlled through the actions of neurotransmitter systems in the cerebral cortex (McCormick et al., 1994). The ‘occipital’ thalamic seed locate in the medial and posterior group of thalamic nuclei, which is connected with the visual cortex and critical for attentional processes (Arend et al., 2015). In hence, we speculated that the ‘somatosensory’ thalamic seed, ‘motor’ thalamic seed and ‘occipital’ thalamic seed involved in attention deficits after SD.
Our findings showed the altered FC between thalamus subregions and left frontal pole, right frontal pole, left middle temporal gyrus (posterior division), right middle temporal gyrus (posterior division), left supramarginal gyrus (anterior division), right supramarginal gyrus (anterior division), and left precuneus. It had been demonstrated that the alerting component involved the thalamic, frontal and parietal areas, the executive attention component involving anterior cingulate cortex and the lateral prefrontal cortex, and the orientating component involving the superior parietal lobe, temporo–parietal junctions and superior frontal cortex (Fan et al., 2005). Our results revealed the dysfunctional cerebral cortices underlying three components of attention performance declines after SD. In line with our results, one previous study revealed the decreased FC between the thalamus and right middle temporal gyrus, right superior frontal gyrus, the right medial frontal gyrus, bilateral middle temporal gyri and left superior frontal gyrus (Shao et al., 2013), which suggested that the thalamus had strong reciprocal connections with the cerebral cortex. Moreover, the altered FC between the right middle temporal gyrus and ‘somatosensory’ thalamic seed was negatively correlated with the change in orienting effect, which suggested the association between the thalamocortical FC and attention performance after SD. Overall, our findings revealed that the altered FC between thalamus subregions and cerebral cortices after SD was associated with impaired attention.
However, there were several limitations to be noted. Firstly, only participants aged between 20 and 30 years were recruited in this study. our results could not be extrapolated to individuals in other age groups. Participants from a broader age range should be recruited in future. Secondly, the sample size was relatively small in our study, which might be the cause of no significant differences on orienting effect and reaction time after SD. Further studies with a larger sample size are needed in future.
Conclusively, we found decreased FC between thalamus subregions and cerebral cortices after SD. Moreover, the altered FC between the right middle temporal gyrus and ‘somatosensory’ thalamic seed was negatively correlated with the change in orienting effect. These findings suggest disruptive changes of the thalamocortical FC after SD, which may lead to the decline of attention.