Disrupted interactions among the hippocampal, dorsal attention, and central‐executive networks in amnestic mild cognitive impairment

Abstract

Neuroimaging investigations consistently demonstrate that the neural processes involve complex interactions between the large‐scale networks. Among those networks, the dorsal attention network (DAN) and the central‐executive network (CEN) have been previously shown to exhibit anti‐correlated activity with the default‐mode network (DMN) in cognitively normal people. In amnestic mild cognitive impairment (MCI) and Alzheimer's disease, the hippocampal network (HCN)—a key memory processing system—and its interactions with other networks have gathered central interest. The current study aims to evaluate the patterns of functional architectures of the HCN with the three networks—DAN, CEN, and DMN—in amnestic MCI and normal controls (NC) to test the hypothesis that the interactions of HCN with other networks alter in MCI. We recorded the resting state functional MRI, assessed patterns of functional architectures between the four networks using dynamical causal modeling, and compared between NC and MCI. Our analysis showed that the DAN modulates the activity between the HCN and the DMN in both MCI and NC. We further uncovered that the DAN modulates the activity between the HCN and the CEN in NC, but such modulation is impaired in MCI. We found an association between impaired modulation and Montreal cognitive assessment (R = 0.349). Overall, our findings provide important insight in understanding the neuroimaging signature of amnestic MCI and/or Alzheimer's disease.

Estimating regional cerebral blood flow using resting-state functional MRI via machine learning

“…RsfMRI has emerged as a commonly acquired MRI protocol primarily used in studies of brain functional connectivity (Biswal et al, 1995;Biswal et al, 2010;Chand et al, 2018;Fox et al, 2014;Greicius and Kimmel, 2012;Raichle, 2015). It indirectly captures the regional neurovascular alterations associated with neuronal activations based on associated changes in deoxyhemoglobin reflecting changes in underlying regional CBF, blood volume, and oxygen metabolism.…”

Self-reference Network-Related Interactions During the Process of Cognitive Impairment in the Early Stages of Alzheimer’s Disease

“…This may be related to the laterality. For instance, the significance of network functional lateralization in AD progression is as follows: (1) in the SN, in which right lateralization has been proven (Zhang et al, 2019 ), the occurrence of connections with the SRN on the right side rather than the left side significantly reduced FC, especially in the right prefrontal cortex, and has been observed in subjective cognitive decline patients (Hu et al, 2017 ); (2) however, in the DAN, damage patterns (Zhang et al, 2015 ) and inhibition in the temporal region of the whole brain have been observed in MCI patients (Chand et al, 2018 ; Zhang et al, 2019 ), but evidence for lateralization remains debatable (Corbetta and Shulman, 2002 ; Vossel et al, 2012 ; Mayrhofer et al, 2019 ); and (3) in addition, the DMN also presented left lateralization but functional decline with age and AD (Banks et al, 2018 ), showing insufficient activation in the right prefrontal region but overactivation in the left prefrontal region during memory maintenance and reasoning tasks in MCI patients (Melrose et al, 2018 ). Nevertheless, the hyperactivation in the DAN and SN and the hypoactivation in the DMN were regarded as compensatory due to damage that had been confirmed to be directly related to the AD pathology in the right hemisphere (Wu et al, 2011 ; Li et al, 2012 ).…”

“…(1) in the SN, in which right lateralization has been proven , the occurrence of connections with the SRN on the right side rather than the left side significantly reduced FC, especially in the right prefrontal cortex, and has been observed in subjective cognitive decline patients (Hu et al, 2017); (2) however, in the DAN, damage patterns (Zhang et al, 2015) and inhibition in the temporal region of the whole brain have been observed in MCI patients (Chand et al, 2018;, but evidence for lateralization remains debatable (Corbetta and Shulman, 2002;Vossel et al, 2012;Mayrhofer et al, 2019); and (3) in addition, the DMN also presented left lateralization but functional decline with age and AD (Banks et al, 2018), showing insufficient activation in the right prefrontal region but overactivation in the left prefrontal FIGURE 3 | The correlation between SRN-related interactions and cognitive functions in mild cognitive impairment patients. The interaction of the SRN with the left DAN was positively correlated with MCI patients' visual-spatial performance in the ECogPT test.…”

“…Regarding interactions with other networks, correlations between emotion and attention to cognition scale performance have been clinically discovered, and self-reference processing may be partially involved (Berkovich-Ohana et al, 2012 ; Amft et al, 2015 ; Catalino et al, 2020 ; Tomova et al, 2020 ; Van der Gucht et al, 2020 ). The dorsal attention network (DAN) and salience network (SN), which function across both high-level cognitive and attention networks (Arkin et al, 2020 ; Shi et al, 2020 ), participate in the regulation of networks between state switching of the brain (Gao and Lin, 2012 ; He et al, 2014 ; Chand et al, 2018 ). Specifically, the right fronto-insular region of the SN plays a critical role in switching between the DMN and the central executive network (He et al, 2014 ), and the DAN modulates the in-between activity and is damaged in MCI; thus, it is responsible for patients’ cognitive impairment (Chand et al, 2018 ).…”

“…The dorsal attention network (DAN) and salience network (SN), which function across both high-level cognitive and attention networks (Arkin et al, 2020 ; Shi et al, 2020 ), participate in the regulation of networks between state switching of the brain (Gao and Lin, 2012 ; He et al, 2014 ; Chand et al, 2018 ). Specifically, the right fronto-insular region of the SN plays a critical role in switching between the DMN and the central executive network (He et al, 2014 ), and the DAN modulates the in-between activity and is damaged in MCI; thus, it is responsible for patients’ cognitive impairment (Chand et al, 2018 ). The actional patterns in AD progression indicate that the mechanisms of healthy cognition and memory are all based on balance.…”