Anterior insular network disconnection and cognitive impairment in Parkinson’s disease

Fathy, Yasmine Y.; Hepp, Dagmar H.; Jong, Frank Jan de; Geurts, Jeroen J. G.; Foncke, E.M.J.; Berendse, Henk W.; Berg, Wilma D. J. van de; Schoonheim, Menno M.

doi:10.1016/j.nicl.2020.102364

Cited by 25 publications

(33 citation statements)

References 39 publications

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“…We also observed lower ALFF values in the left insula in the PD-Post-DBS group. The insular lobe was thought to regulate DMN, as well as the fronto-parietal network ( Fathy et al, 2020 ), and is associated with cognitive impairment in PD ( Deen et al, 2011 ; Fathy et al, 2020 ). After STN-DBS, the cognitive decline on frontal executive function ( Mikos et al, 2011 ; Lefaucheur et al, 2012 ), particularly verbal fluency ( Okun et al, 2009 ; Mikos et al, 2011 ; Lefaucheur et al, 2012 ), found in many studies is considered to be due to the surgical microlesion ( Mikos et al, 2011 ; Lefaucheur et al, 2012 ).…”

Section: Discussionmentioning

confidence: 99%

Altered Spontaneous Neural Activity and Functional Connectivity in Parkinson’s Disease With Subthalamic Microlesion

et al. 2021

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BackgroundTransient improvement in motor symptoms are immediately observed in patients with Parkinson’s disease (PD) after an electrode has been implanted into the subthalamic nucleus (STN) for deep brain stimulation (DBS). This phenomenon is known as the microlesion effect (MLE). However, the underlying mechanisms of MLE is poorly understood.PurposeWe utilized resting state functional MRI (rs-fMRI) to evaluate changes in spontaneous brain activity and networks in PD patients during the microlesion period after DBS.MethodOverall, 37 PD patients and 13 gender- and age-matched healthy controls (HCs) were recruited for this study. Rs-MRI information was collected from PD patients three days before DBS and one day after DBS, whereas the HCs group was scanned once. We utilized the amplitude of low-frequency fluctuation (ALFF) method in order to analyze differences in spontaneous whole-brain activity among all subjects. Furthermore, functional connectivity (FC) was applied to investigate connections between other brain regions and brain areas with significantly different ALFF before and after surgery in PD patients.ResultRelative to the PD-Pre-DBS group, the PD-Post-DBS group had higher ALFF in the right putamen, right inferior frontal gyrus, right precentral gyrus and lower ALFF in right angular gyrus, right precuneus, right posterior cingulate gyrus (PCC), left insula, left middle temporal gyrus (MTG), bilateral middle frontal gyrus and bilateral superior frontal gyrus (dorsolateral). Functional connectivity analysis revealed that these brain regions with significantly different ALFF scores demonstrated abnormal FC, largely in the temporal, prefrontal cortices and default mode network (DMN).ConclusionThe subthalamic microlesion caused by DBS in PD was found to not only improve the activity of the basal ganglia-thalamocortical circuit, but also reduce the activity of the DMN and executive control network (ECN) related brain regions. Results from this study provide new insights into the mechanism of MLE.

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Section: Discussionmentioning

confidence: 99%

Altered Spontaneous Neural Activity and Functional Connectivity in Parkinson’s Disease With Subthalamic Microlesion

et al. 2021

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“…CAMCOG_Total: Cambridge Cognitive Battery Total score, H&Y: Hoehn and Yahr stage, ISCED: International Standard Classification of Education, LEDD: Levodopa equivalent daily dose, PD: Parkinson’s disease, SD: Standard Deviation, UPDRS III: Unified Parkinson’s Disease Rating Scale part III, LEDD: L-DOPA equivalent daily dose.. ^mean and range is reported for these variables.. * p < 0.05, ** p < 0.01. Table adapted from Fathy et al, 2020 28 .…”

Section: Resultsmentioning

confidence: 99%

“…The anterior insula has strong connections with the ACC 13 , and is associated with cognitive control in PD 28 . Since only the dAI, not the vAI, showed network topological alterations of eigenvector and betweenness centrality in PD, we assessed microstructural alteration in the connections between the dAI and ACC only.…”

Section: Resultsmentioning

confidence: 99%

“…The main strength of our study is the region-specific approach, based on functional associations within the salience network, specifically the anterior insula and ACC 28 . There are however, several limitations that need to be addressed.…”

Section: Discussionmentioning

confidence: 99%

“…Within the salience network, connections between the AIC and ACC are important for rapid orientation of attention and adaptive switching of cognitive control 13 , 21 , 24 – 26 . There is strong evidence that functional changes in the salience network are related to cognitive impairment and depression in PD, but structurally this network remains understudied 27 , 28 . Therefore, the aim of the current study is to address the structural centrality of the dAI and vAI, as well as the microstructural integrity of tracts between the dAI, vAI and ACC, in relation to cognitive and affective functions in PD patients and healthy controls.…”

Section: Introductionmentioning

confidence: 99%

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Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease

Jonkman

Fathy

Berendse

et al. 2021

Sci Rep

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The aim of the current study was to assess the structural centrality and microstructural integrity of the cortical hubs of the salience network, the anterior insular cortex (AIC) subregions and anterior cingulate cortex (ACC), and their relationship to cognitive and affective impairment in PD. MRI of 53 PD patients and 15 age-matched controls included 3D-T1 for anatomical registration, and diffusion tensor imaging for probabilistic tractography. Network topological measures of eigenvector and betweenness centrality were calculated for ventral (vAI) and dorsal (dAI) AIC. Microstructural tract integrity between vAI, dAI and the ACC was quantified with fractional anisotrophy (FA) and mean diffusivity (MD). Structural integrity and connectivity were related to cognitive and affective scores. The dAI had significantly higher eigenvector centrality in PD than controls (p < 0.01), associated with higher depression scores (left dAI only, rs = 0.28, p < 0.05). Tracts between dAI and ACC showed lower FA and higher MD in PD (p < 0.05), and associated with lower semantic fluency, working memory and executive functioning, and higher anxiety scores (range 0.002 < p < 0.05). This study provides evidence for clinically relevant structural damage to the cortical hubs of the salience network in PD, possibly due to extensive local neuropathology and loss of interconnecting AIC-ACC tracts.

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Brain connectivity markers in advanced Parkinson’s disease for predicting mild cognitive impairment

et al. 2021

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Anterior insular network disconnection and cognitive impairment in Parkinson’s disease

Abstract: Graphical abstract

Cited by 25 publications

References 39 publications

Altered Spontaneous Neural Activity and Functional Connectivity in Parkinson’s Disease With Subthalamic Microlesion

Altered Spontaneous Neural Activity and Functional Connectivity in Parkinson’s Disease With Subthalamic Microlesion

Structural network topology and microstructural alterations of the anterior insula associate with cognitive and affective impairment in Parkinson’s disease

Brain connectivity markers in advanced Parkinson’s disease for predicting mild cognitive impairment

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