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European Review for Medical and Pharmacological Sciences 2021; 25: 2031-2038 Abnormal ventral attention network homogeneity in patients with right temporal lobe epilepsy D.-B. LI1,2, R.-S. LIU3, X. WANG4, P.-A. XIONG5, H.-W. REN6, Y.-F. WEI2, L.-M. ZHANG1, Y.-J. GAO7 1Department of Neurology, The First Affiliated Hospital of Harbin Medical University, Harbin, China 2First Department of Neurology and Neuroscience Center, Heilongjiang Provincial Hospital, Harbin, China 3Department of Neurology, The Fourth Affiliated Hospital of Harbin Medical University, Harbin, China 4Department of Mental Health, Taihe Hospital, Hubei University of Medicine, Shiyan, China 5Department of Taihe Hospital Reproductive Medicine Center Affiliated to Hubei University of Medicine, Shiyan, China 6Department of Medical Imaging, Tianyou Hospital Affiliated to Wuhan University of Science and Technology, Wuhan, China 7Department of Psychiatry, Tianyou Hospital Affiliated to Wuhan University of Science and Technology, Wuhan, China Dongbin Li and Ruoshi Liu contributed equally to this work Abstract. – OBJECTIVE: The attention net- to the pathophysiology of cognitive impairment work is the structural basis of cognitive func- in rTLE. tion. As one of the two known attention net- works, the ventral attention network (VAN) has Key Words: a significant impact on the cognitive impairment Right temporal lobe epilepsy, Ventral attention net- of patients with epilepsy. Nevertheless, changes work, Network homogeneity, Resting-state function- in network homogeneity (NH) are rarely reported al magnetic resonance imaging. in the VAN of right temporal lobe epilepsy (rTLE) patients. Therefore, we explored the NH of the VAN in rTLE patients in this study. PATIENTS AND METHODS: Seventy rTLE pa- Introduction tients and 69 healthy controls were recruited. All participants underwent resting-state functional magnetic resonance imaging (fMRI), which was Epilepsy is a severe brain condition, characte- the primary method of evaluation. The executive rized by the recurrence of seizures, and results in control reaction time (ECRT) was examined via a massive burden on the healthcare infrastructure the attentional network test. The Data Process- and economy1. As one of the most common forms ing Assistant for Resting-State fMRI (DPARSF) of focal epilepsy, temporal lobe epilepsy (TLE) is was used to analyze NH. The independent com- characterized by cognitive dysfunctions and re- ponent analysis (ICA) and correlation analysis 2 were used in data analysis. fractoriness . With the advent of new and widely RESULTS: Compared to the control group, pa- applied imaging techniques, structural abnor- tients with right temporal lobe epilepsy showed malities in several brain regions of patients with a lower NH in the right superior temporal gyrus, epilepsy have been identified. TLE was confir- and a longer ECRT. However, abnormal NH val- med as a condition associated with network-level ues had no significant association with the clin- destruction3. Increasing evidence, provided by ical measurements. resting-state functional magnetic resonance ima- CONCLUSIONS: Patients with right tempo- ral lobe epilepsy have abnormal NH values in ging studies (fMRI), has also confirmed the pre- the VAN, and the executive functions in rTLE sence of neural connections, which were thought patients are also altered. The altered NH val- to be the most direct approach to functional con- ues in VAN may help provide new insights in- nectivity among separated regions of the brain at Corresponding Authors: Liming Zhang, MD; e-mail: [email protected] Yujun Gao, e-mail: [email protected] 2031 D.-B. Li, R.-S. Liu, X. Wang, P.-A. Xiong, H.-W. Ren, Y.-F. Wei, L.-M. Zhang, Y.-J. Gao rest. Thus, fMRI analysis is the primary method been reported. Therefore, we measured the diffe- for research into brain networks. rences in the NH values of the VAN between the The ventral attention network (VAN) is a rTLE patients and healthy controls and investiga- resting-state network and an array of brain re- ted the potential mechanism of impaired attention gions in the right cerebral hemisphere are cen- function of rTLE. tered on the temporo-parietal junction (TPJ) and the ventrolateral prefrontal cortex4. As one of the two well-known attention networks in the Patients and Methods human brain, the VAN modulates bottom-up “exogenous” attention, which directs attention Patients to an unexpected stimulus. When an unexpected Seventy patients with rTLE were recruited from event occurs, the VAN activates and generates the Department of Psychiatry, Tianyou Hospital an “interrupt signal” to break the current focus Affiliated to Wuhan University of Science and of attention and reallocate attention to a new Technology. Sixty-nine healthy people were recru- spatial location5. The VAN has been reported ited from those who underwent a standard physical to correlate with cognition, information proces- examination at the medical examination center of sing speed, emotion regulation, depression, and the Tianyou Hospital Affiliated to Wuhan Uni- anxiety6-8. Because of its location, structure, and versity of Science and Technology. Seventy rTLE function, the VAN has been reported to be highly patients were diagnosed according to the Interna- associated with many neuropsychiatric disorders, tional League Against Epilepsy25. The inclusion including Alzheimer’s, schizophrenia, and autism criteria for the rTLE were as follows (epilepsy spectrum disorder9-11. Recent works have found patients who met any two of the following symp- that cognitive impairment and attention deficit toms): (1) the clinical onset of symptoms suggested are prominent in epileptic patients12,13, and, as epileptic foci in the temporal lobe, such as psychia- the basis of advanced nervous function, attention tric symptoms, abnormal emotional experiences, function plays an essential role in cognitive pro- automatisms, epigastric rising, or dystonic postu- cessing. Considering the importance of the VAN, ring of the limbs; (2) the interictal electroencepha- which is associated with attention functioning, lographic traces suggested abnormality in the right especially visual-spatial attention14,15, studies on temporal lobe; and (3) the imaging results showed the action of the VAN in epileptic patients would atrophy or sclerosis in the right hippocampus. The be important. As a survey method, network ho- exclusion criteria for all subjects were as follows: mogeneity (NH) was thought to be an ideal (1) structural MRI finding identifiable focal abnor- parameter with which to assess the connectivi- malities other than hippocampal sclerosis atrophy; ty of brain networks in many neuropsychiatric (2) left-handed; (3) any lifetime psychiatric di- diseases, such as attention-deficit/hyperactivity sorder; (4) history of serious medical diseases or disorder, schizophrenia, and somatization16-24. As other neurological illness; and (5) Mini-Mental a voxel-wise survey, NH correlates with other State Examination scores ≤ 24. All subjects gave voxels within a given network, and can be uti- written, informed consent before participating in lized to assess the connectivity of a voxel with the study. Our study was performed according to the other brain voxels of a predefined network. the Declaration of Helsinki and approved by the NH is defined as the average connectivity of Medical Ethics Committee of the Tianyou Hospi- any specific time series of a voxel with the time tal Affiliated to Wuhan University of Science and series of every other voxel in the network. With Technology. this approach, compromised network homogenei- ty in brain regions of a specific disease can be Behavioral Paradigm identified17. As NH combines the advantages of The executive function was assessed by the 26 the region-of-interest, seed-based functional con- attentional network test (ANT) . “In the center nectivity method and the independent component of the testing screen, four cue signals indicating analysis method, it offers an unbiased, hypothe- forthcoming target signals consisted of a double sis-driven measure of a given brain network. asterisk, a central asterisk, an asterisk above or Thus, group differences can be identified without below, and no asterisk. Arrows could appear in the need for a priori knowledge of where in the one of the following: one target arrow in the cen- network abnormalities might be16. However, the ter and another four arrows for interference. Two VAN homogeneity in patients with rTLE has not different directions randomly appeared between 2032 Abnormal ventral attention network homogeneity in patients with right temporal lobe epilepsy the central and interfering arrows in congruent or Ventral Attention Network Identification incongruent directions. Participants were requi- The GIFT toolbox32 was used to select VAN as red to quickly and correctly determine the target a mask from all participants through the group orientation. Reaction time (RT) was then recor- ICA method. We used three steps from the GIFT ded by the ANT software, and by subtracting the toolbox as follows: data reduction; independent consistent arrow direction RT from the inconsi- component separation; and back reconstruction. stent arrow direction RT, the executive control When every component was considered, a sta- reaction time (ECRT) was calculated. tistical map was generated and threshold by a The detailed steps which are quoted in this pa- voxel-wise, one-sample t-test (p<0.01 for multiple ragraph were excerpted from our previous study27.