Cerebellar functional activity alteration in right temporal lobe epilepsy patients with different level of executive function: the fractional amplitude of low-frequency fluctuation combined with functional connectivity analysis_Journal of Epilepsy

Authors：

ZHOU Xia ¹ , LI Chunyan ¹ , FAN Binglin ² , CHEN Junyi ¹ , LI Shenghua ¹ , QUAN Xuemei ¹ , YI Zufang ¹ ,  ZHENG Jinou ³

1. Department of Neurology, Guangxi Academy of Medical Sciences, the People’s Hospital of Guangxi Zhuang Autonomous Region, Nanning 530021, China;
2. Department of Geriatric Neurology, Guangxi Academy of Medical Sciences, the People’s Hospital of Guangxi Zhuang Autonomous region, 530021, Nanning, China;
3. Department of Neurology, the First Affiliated Hospital of Guangxi Medical University, Nanning 530021, China;

Corresponding?author：

ZHENG Jinou, Email: jinouzheng@163.com

Keywords：

Fractional amplitude of low-frequency fluctuation; Functional connectivity; Temporal lobe epilepsy; Functional magnetic resonance imaging

DOI：

10.7507/2096-0247.202601001

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective Aimed to investigate the local neural activity and functional connectivity (FC) in the whole brain of cerebellum by fractional amplitude of low-frequency fluctuation (fALFF) and seed-based FC in right temporal lobe epilepsy (rTLE) patients with different level of executive function. Methods 20 healthy controls (HC), 18 rTLE patients with executive nonimpairment (ENI) and 20 rTLE patients with executive impairment (EI) were enrolled. The resting-functional magnetic resonance imaging (rs-fMRI) data of every participant was collected. The local neural activity in the cerebellum was analyzed by fALFF; the cerebral regions with significant zfALFF values among groups were selected as seeds for subsequent FC analyses in the whole brain. Results The fALFF analysis showed that the significantly differential cerebellar regions were located in right cerebellum lobule VIII and left cerebellum lobule VI. Compared with the HC group, the neural functional activity of right cerebellum lobule VIII was increased in the NEI-rTLE and EI-rTLE groups, but no difference between the patient groups. Compared with the HC group, the functional activity of left cerebellum lobule VI was increased in the ENI-rTLE group, decreased in the EI-rTLE group. The further FC analysis showed altered FCs between right cerebellum lobule VIII and right cerebellum lobule IX, right inferior orbitofrontal gyrus, right middle forbitorontal gyrus, right superior frontal gyrus, left middle frontal gyrus and left inferior parietal gyrus, which were increased in the ENI-rTLE patient group while increased and decreased in the EI-rTLE group. Conclusion The rTLE patients showed that functional activity of cerebellum in the local and whole brain were reorganized, and the cerebellum exerted compensatory and decompensated role in the process of cognitive impairment.

Citation： ZHOU Xia, LI Chunyan, FAN Binglin, CHEN Junyi, LI Shenghua, QUAN Xuemei, YI Zufang, ZHENG Jinou. Cerebellar functional activity alteration in right temporal lobe epilepsy patients with different level of executive function: the fractional amplitude of low-frequency fluctuation combined with functional connectivity analysis. Journal of Epilepsy, 2026, 12(2): 93-100. doi: 10.7507/2096-0247.202601001 Copy

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2.	Pope RA, Thompson PJ, Rantell K, et al. Frontal lobe dysfunction as a predictor of depression and anxiety following temporal lobe epilepsy surgery. Epilepsy Res, 2019, 152(1): 59-66.
3.	Limotai C, McLachlan RS, Hayman-Abello S, et al. Memory loss and memory reorganization patterns in temporal lobe epilepsy patients undergoing anterior temporal lobe resection, as demonstrated by pre-versus post-operative functional MRI. J Clin Neurosci, 2018, 55(1): 38-44.
4.	Bao Y, He R, Zeng Q, et al. Investigation of microstructural abnormalities in white and gray matter around hippocampus with diffusion tensor imaging (DTI) in temporal lobe epilepsy (TLE). Epilepsy Behav, 2018, 83: 44-49.
5.	Beheshti I, Sone D, Farokhian F, et al. Gray matter and white matter abnormalities in temporal lobe epilepsy patients with and without hippocampal sclerosis. Front Neurol, 2018, 9(1): 107.
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9.	Guo L, Bai G, Zhang H, et al. Cognitive functioning in temporal lobe epilepsy: a BOLD-fMRI study. Mol Neurobiol, 2017, 54(24): 8361-8369.
10.	Zhang Z, Liao W, Xu Q, et al. Hippocampus-associated causal network of structural covariance measuring structural damage progression in temporal lobe epilepsy. Hum Brain Mapp, 2017, 38(3): 753-766.
11.	Liao H, Liao M, Xu L, et al. Integrative analysis of h-prune as a potential therapeutic target for hepatocellular carcinoma. E Bio Medicine, 2019, 41(2): 310-319.
12.	Grant RW, O'Brien KE, Waxler JL, et al. Personalized genetic risk counseling to motivate diabetes prevention: a randomized trial. Diabetes Care, 2013, 36(1): 13-19.
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14.	Huang H, Huang D, Luo C, et al. Abnormalities of regional brain activity and executive function in patients with temporal lobe epilepsy: a cross-sectional and longitudinal resting-state functional MRI study. Neuroradiology, 2024, 66(5): 1093-1104.
15.	Qin L, Jiang W, Zheng J, et al. Alterations functional connectivity in temporal lobe epilepsy and their relationships with cognitive function: a longitudinal resting-state fMRI study. Front Neurol, 2020, 11(3): 625.
16.	鄭金甌, 黨超, 梁志堅, 等. 顳葉癲癇患者執行功能的功能磁共振研究. 中國神經精神疾病雜志, 2011, 37: 166-170.
17.	Specht K, Lie CH, Shah NJ, et al. Disentangling the prefrontal network for rule selection by means of a non-verbal variant of the Wisconsin Card Sorting Test. Hum Brain Mapp, 2009, 30(11): 1734-1743.
18.	Beratis IN, Rabavilas AD, Kyprianou M, et al. Investigation of the link between higher order cognitive functions and handedness. J Clin Exp Neuropsychol, 2013, 35(2): 393-403.
19.	Liu J, Zhou X, Zhang Z, et al. Disrupted functional network in patients with temporal lobe epilepsy with impaired alertness. Epilepsy Behav, 2019, 101: 106573.
20.	Yang H, Zhang C, Liu C, et al. Brain network alteration in patients with temporal lobe epilepsy with cognitive impairment. Epilepsy Behav, 2018, 81: 41-48.
21.	Zhang C, Yang H, Qin W, et al. Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci, 2017, 11(3): 609.
22.	Bernard JA, Peltier SJ, Benson BL, et al. Dissociable functional networks of the human dentate nucleus. Cereb Cortex, 2014, 24(12): 2151-2159.
23.	Habas C, Kamdar N, Nguyen D, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci, 2009, 29(20): 8586-8594.
24.	Krienen FM, Buckner RL Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex, 2009, 19(11): 2485-2497.
25.	Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage, 2009, 44(2): 489-501.
26.	Solstrand Dahlberg L, Lungu O, Doyon J. Cerebellar contribution to motor and non-motor functions in Parkinson's Disease: a meta-analysis of fMRI findings. Front Neurol, 2020, 11(1): 127.
27.	Kim T, Lee KH, Oh H, et al. Cerebellar structural abnormalities associated with cognitive function in patients with first-episode psychosis. Front Psychiatry, 2018, 9(1): 286.
28.	Zhang Z, Lu G, Zhong Y, et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res, 2010, 1323: 152-160.
29.	Ofer I, LeRose C, Mast H, et al. Association between seizure freedom and default mode network reorganization in patients with unilateral temporal lobe epilepsy. Epilepsy Behav, 2019, 90: 238-246.
30.	Jiang Y, Liu DF, Zhang X, et al. Microstructure and functional connectivity-based evidence for memory-related regional impairments in the brains of pilocarpine-treated rats. Brain Res Bull, 2020, 154(1): 127-134.
31.	Lv ZX, Huang DH, Ye W, et al. Alteration of functional connectivity within visuospatial working memory-related brain network in patients with right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav, 2014, 35: 64-71.
32.	Huang W, Huang D, Chen Z, et al. Alterations in the functional connectivity of a verbal working memory-related brain network in patients with left temporal lobe epilepsy. Neurosci Lett, 2015, 602(1): 6-11.
33.	Holmes M, Folley BS, Sonmezturk HH, et al. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp, 2014, 35(3): 735-744.
34.	Zhang Z, Zhou X, Liu J, et al. Aberrant executive control networks and default mode network in patients with right-sided temporal lobe epilepsy: a functional and effective connectivity study. Int J Neurosci, 2020, 130(3): 683-693.
35.	Li X, Liang Y, Chen Y, et al. Disrupted frontoparietal network mediates white matter structure dysfunction associated with cognitive decline in hypertension patients. J Neurosci, 2015, 35(24): 10015-10024.
36.	Forn C, Rocca MA, Valsasina P, et al. Functional magnetic resonance imaging correlates of cognitive performance in patients with a clinically isolated syndrome suggestive of multiple sclerosis at presentation: an activation and connectivity study. Mult Scler, 2012, 18(1): 153-163.

1. Orjuela-Rojas JM, Martinez-Juarez IE, Ruiz-Chow A, et al. Treatment of depression in patients with temporal lobe epilepsy: a pilot study of cognitive behavioral therapy vs. selective serotonin reuptake inhibitors. Epilepsy Behav, 2015, 51: 176-181.
2. Pope RA, Thompson PJ, Rantell K, et al. Frontal lobe dysfunction as a predictor of depression and anxiety following temporal lobe epilepsy surgery. Epilepsy Res, 2019, 152(1): 59-66.
3. Limotai C, McLachlan RS, Hayman-Abello S, et al. Memory loss and memory reorganization patterns in temporal lobe epilepsy patients undergoing anterior temporal lobe resection, as demonstrated by pre-versus post-operative functional MRI. J Clin Neurosci, 2018, 55(1): 38-44.
4. Bao Y, He R, Zeng Q, et al. Investigation of microstructural abnormalities in white and gray matter around hippocampus with diffusion tensor imaging (DTI) in temporal lobe epilepsy (TLE). Epilepsy Behav, 2018, 83: 44-49.
5. Beheshti I, Sone D, Farokhian F, et al. Gray matter and white matter abnormalities in temporal lobe epilepsy patients with and without hippocampal sclerosis. Front Neurol, 2018, 9(1): 107.
6. Ahmadian N, van Baarsen K, van Zandvoort M, et al. The cerebellar cognitive affective syndrome-a meta-analysis. Cerebellum, 2019, 18(4): 941-950.
7. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain, 1998, 121 ( Pt 4): 561-579.
8. Li J, Chen X, Ye W, et al. Alteration of the alertness-related network in patients with right temporal lobe epilepsy: a resting state fMRI study. Epilepsy Res, 2016, 127(2): 252-259.
9. Guo L, Bai G, Zhang H, et al. Cognitive functioning in temporal lobe epilepsy: a BOLD-fMRI study. Mol Neurobiol, 2017, 54(24): 8361-8369.
10. Zhang Z, Liao W, Xu Q, et al. Hippocampus-associated causal network of structural covariance measuring structural damage progression in temporal lobe epilepsy. Hum Brain Mapp, 2017, 38(3): 753-766.
11. Liao H, Liao M, Xu L, et al. Integrative analysis of h-prune as a potential therapeutic target for hepatocellular carcinoma. E Bio Medicine, 2019, 41(2): 310-319.
12. Grant RW, O'Brien KE, Waxler JL, et al. Personalized genetic risk counseling to motivate diabetes prevention: a randomized trial. Diabetes Care, 2013, 36(1): 13-19.
13. Fan J, McCandliss BD, Sommer T, et al. Testing the efficiency and independence of attentional networks. J Cogn Neurosci, 2002, 14(2): 340-347.
14. Huang H, Huang D, Luo C, et al. Abnormalities of regional brain activity and executive function in patients with temporal lobe epilepsy: a cross-sectional and longitudinal resting-state functional MRI study. Neuroradiology, 2024, 66(5): 1093-1104.
15. Qin L, Jiang W, Zheng J, et al. Alterations functional connectivity in temporal lobe epilepsy and their relationships with cognitive function: a longitudinal resting-state fMRI study. Front Neurol, 2020, 11(3): 625.
16. 鄭金甌, 黨超, 梁志堅, 等. 顳葉癲癇患者執行功能的功能磁共振研究. 中國神經精神疾病雜志, 2011, 37: 166-170.
17. Specht K, Lie CH, Shah NJ, et al. Disentangling the prefrontal network for rule selection by means of a non-verbal variant of the Wisconsin Card Sorting Test. Hum Brain Mapp, 2009, 30(11): 1734-1743.
18. Beratis IN, Rabavilas AD, Kyprianou M, et al. Investigation of the link between higher order cognitive functions and handedness. J Clin Exp Neuropsychol, 2013, 35(2): 393-403.
19. Liu J, Zhou X, Zhang Z, et al. Disrupted functional network in patients with temporal lobe epilepsy with impaired alertness. Epilepsy Behav, 2019, 101: 106573.
20. Yang H, Zhang C, Liu C, et al. Brain network alteration in patients with temporal lobe epilepsy with cognitive impairment. Epilepsy Behav, 2018, 81: 41-48.
21. Zhang C, Yang H, Qin W, et al. Characteristics of resting-state functional connectivity in intractable unilateral temporal lobe epilepsy patients with impaired executive control function. Front Hum Neurosci, 2017, 11(3): 609.
22. Bernard JA, Peltier SJ, Benson BL, et al. Dissociable functional networks of the human dentate nucleus. Cereb Cortex, 2014, 24(12): 2151-2159.
23. Habas C, Kamdar N, Nguyen D, et al. Distinct cerebellar contributions to intrinsic connectivity networks. J Neurosci, 2009, 29(20): 8586-8594.
24. Krienen FM, Buckner RL Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex, 2009, 19(11): 2485-2497.
25. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage, 2009, 44(2): 489-501.
26. Solstrand Dahlberg L, Lungu O, Doyon J. Cerebellar contribution to motor and non-motor functions in Parkinson's Disease: a meta-analysis of fMRI findings. Front Neurol, 2020, 11(1): 127.
27. Kim T, Lee KH, Oh H, et al. Cerebellar structural abnormalities associated with cognitive function in patients with first-episode psychosis. Front Psychiatry, 2018, 9(1): 286.
28. Zhang Z, Lu G, Zhong Y, et al. Altered spontaneous neuronal activity of the default-mode network in mesial temporal lobe epilepsy. Brain Res, 2010, 1323: 152-160.
29. Ofer I, LeRose C, Mast H, et al. Association between seizure freedom and default mode network reorganization in patients with unilateral temporal lobe epilepsy. Epilepsy Behav, 2019, 90: 238-246.
30. Jiang Y, Liu DF, Zhang X, et al. Microstructure and functional connectivity-based evidence for memory-related regional impairments in the brains of pilocarpine-treated rats. Brain Res Bull, 2020, 154(1): 127-134.
31. Lv ZX, Huang DH, Ye W, et al. Alteration of functional connectivity within visuospatial working memory-related brain network in patients with right temporal lobe epilepsy: a resting-state fMRI study. Epilepsy Behav, 2014, 35: 64-71.
32. Huang W, Huang D, Chen Z, et al. Alterations in the functional connectivity of a verbal working memory-related brain network in patients with left temporal lobe epilepsy. Neurosci Lett, 2015, 602(1): 6-11.
33. Holmes M, Folley BS, Sonmezturk HH, et al. Resting state functional connectivity of the hippocampus associated with neurocognitive function in left temporal lobe epilepsy. Hum Brain Mapp, 2014, 35(3): 735-744.
34. Zhang Z, Zhou X, Liu J, et al. Aberrant executive control networks and default mode network in patients with right-sided temporal lobe epilepsy: a functional and effective connectivity study. Int J Neurosci, 2020, 130(3): 683-693.
35. Li X, Liang Y, Chen Y, et al. Disrupted frontoparietal network mediates white matter structure dysfunction associated with cognitive decline in hypertension patients. J Neurosci, 2015, 35(24): 10015-10024.
36. Forn C, Rocca MA, Valsasina P, et al. Functional magnetic resonance imaging correlates of cognitive performance in patients with a clinically isolated syndrome suggestive of multiple sclerosis at presentation: an activation and connectivity study. Mult Scler, 2012, 18(1): 153-163.

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