Neural mechanisms of fear responses to emotional stimuli: a preliminary study combining early posterior negativity and electroencephalogram source network analysis_Journal of Biomedical Engineering

Authors：

ZANG Qian ^1,2 , ZHAO Xiaoming ^2,3 ,  LIANG Tie ^2,3,4 , LIU Xiuling ^2,3 ,  LOU Cunguang ^2,3

1. Center for Student Mental Health and Development, Hebei University, Baoding, Hebei 071002, P. R. China;
2. Key Laboratory of Digital Medical Engineering of Hebei Province, Hebei University, Baoding, Hebei 071002, P. R. China;
3. College of Electronic and Information Engineering, Hebei University, Baoding, Hebei 071002, P.R.China;
4. Guangxi Health Commission Key Laboratory of Basic Research on Brain Function and Disease, Guangxi Medical University, Nanning 530021, P. R. China;

Corresponding author：

LIANG Tie, Email: hbuliangtie@163.com; LOU Cunguang, Email: loucunguang@163.com

Keywords：

Fear; Early posterior negativity; Electroencephalogram source analysis; Negative emotion

DOI：

10.7507/1001-5515.202403052

Video：

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Abstract Full text Figures/Tables Video References Cited by

Fear emotion is a typical negative emotion that is commonly present in daily life and significantly influences human behavior. A deeper understanding of the mechanisms underlying negative emotions contributes to the improvement of diagnosing and treating disorders related to negative emotions. However, the neural mechanisms of the brain when faced with fearful emotional stimuli remain unclear. To this end, this study further combined electroencephalogram (EEG) source analysis and cortical brain network construction based on early posterior negativity (EPN) analysis to explore the differences in brain information processing mechanisms under fearful and neutral emotional picture stimuli from a spatiotemporal perspective. The results revealed that neutral emotional stimuli could elicit higher EPN amplitudes compared to fearful stimuli. Further source analysis of EEG data containing EPN components revealed significant differences in brain cortical activation areas between fearful and neutral emotional stimuli. Subsequently, more functional connections were observed in the brain network in the alpha frequency band for fearful emotions compared to neutral emotions. By quantifying brain network properties, we found that the average node degree and average clustering coefficient under fearful emotional stimuli were significantly larger compared to neutral emotions. These results indicate that combining EPN analysis with EEG source component and brain network analysis helps to explore brain functional modulation in the processing of fearful emotions with higher spatiotemporal resolution, providing a new perspective on the neural mechanisms of negative emotions.

Citation： ZANG Qian, ZHAO Xiaoming, LIANG Tie, LIU Xiuling, LOU Cunguang. Neural mechanisms of fear responses to emotional stimuli: a preliminary study combining early posterior negativity and electroencephalogram source network analysis. Journal of Biomedical Engineering, 2024, 41(5): 951-957. doi: 10.7507/1001-5515.202403052 Copy

1.	胡素. 情绪面孔启动情绪的神经基础: 来自大脑诱发和自发神经活动模式的证据. 杭州: 浙江师范大学, 2023.
2.	王静, 田小霖, 王雄飞, 等. 基于立体定向脑电图记录恐惧情绪的神经网络研究. 中国现代神经疾病杂志, 2023, 23(3): 189-195.
3.	Zidda F, Andoh J, Pohlack S, et al. Default mode network connectivity of fear-and anxiety-related cue and context conditioning. NeuroImage, 2018, 165: 190-199.
4.	Stark R, Schienle A, Walter B, et al. Hemodynamic responses to fear and disgust-inducing pictures: an fMRI study. Int J Psychophysiol, 2003, 50(3): 225-234.
5.	Landová E, Rádlová S, Pidnebesna A, et al. Toward a reliable detection of arachnophobia: subjective, behavioral, and neurophysiological measures of fear response. Front Psychiatry, 2023, 14: 1196785.
6.	Kroes M C W, Dunsmoor J E, Hakimi M, et al. Patients with dorsolateral prefrontal cortex lesions are capable of discriminatory threat learning but appear impaired in cognitive regulation of subjective fear. Soc Cogn Affect Neur, 2019, 14(6): 601-612.
7.	Dilger S, Straube T, Mentzel H J, et al. Brain activation to phobia-related pictures in spider phobic humans: an event-related functional magnetic resonance imaging study. Neurosci Lett, 2003, 348(1): 29-32.
8.	Schupp H T, Stockburger J, Codispoti M, et al. Stimulus novelty and emotion perception: the near absence of habituation in the visual cortex. Neuroreport, 2006, 17(4): 365-369.
9.	Ding R, Li P, Wang W, et al. Emotion processing by ERP combined with development and plasticity. Neural Plast, 2017, 2017: 5282670.
10.	Schupp H T, Kirmse U M. Case-by-case: Emotional stimulus significance and the modulation of the EPN and LPP. Psychophysiology, 2021, 58(4): e13766.
11.	Aldunate N, López V, Bosman C A. Early influence of affective context on emotion perception: EPN or Early-N400?. Front Neurosci, 2018, 12: 413585.
12.	Van Strien J W, Van der Peijl M K. Enhanced early visual processing in response to snake and trypophobic stimuli. BMC psychology, 2018, 6: 1-8.
13.	Langeslag S J E, Van Strien J W. Early visual processing of snakes and angry faces: an ERP study. Brain Res, 2018, 1678: 297-303.
14.	Zhou F, Zhao W, Qi Z, et al. A distributed fMRI-based signature for the subjective experience of fear. Nat Commun, 2021, 12(1): 6643.
15.	Stefanescu M R, Endres R J, Hilbert K, et al. Networks of phobic fear: Functional connectivity shifts in two subtypes of specific phobia. Neurosci Lett, 2018, 662: 167-172.
16.	Hassan M, Wendling F. Electroencephalography source connectivity: aiming for high resolution of brain networks in time and space. IEEE Signal Proc Mag, 2018, 35(3): 81-96.
17.	Grech R, Cassar T, Muscat J, et al. Review on solving the inverse problem in EEG source analysis. J Neuroeng Rehabil, 2008, 5: 1-33.
18.	Trettin M, Dvoák J, Hilke M, et al. Neuronal response to high negative affective stimuli in major depressive disorder: An fMRI study. J Affect Disorders, 2022, 298: 239-247.
19.	尹宁, 张家皓, 王海力, 等. 磁刺激穴位调节负性情绪的脑电溯源和脑网络研究. 电工技术学报, 2021, 36(4): 756-764.
20.	Thom N, Knight J, Dishman R, et al. Emotional scenes elicit more pronounced self-reported emotional experience and greater EPN and LPP modulation when compared to emotional faces. Cogn Affect Behav Ne, 2014, 14: 849-860.
21.	Zhang Y, Chen S, Deng Z, et al. Benefits of implicit regulation of instructed fear: Evidence from neuroimaging and functional connectivity. Front Neurosci, 2020, 14: 514367.
22.	Milad M R, Wright C I, Orr S P, et al. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiat, 2007, 62(5): 446-454.
23.	Kummar A S, Correia H, Fujiyama H. A brief review of the EEG literature on mindfulness and fear extinction and its potential implications for posttraumatic stress symptoms (PTSS). Brain Sci, 2019, 9(10): 258.
24.	Maffei A, Coccaro A, Jaspers-Fayer F, et al. EEG alpha band functional connectivity reveals distinct cortical dynamics for overt and covert emotional face processing. Sci Rep, 2023, 13(1): 9951.
25.	Bacigalupo F, Luck S J. Alpha-band EEG suppression as a neural marker of sustained attentional engagement to conditioned threat stimuli. Soc Cogn Affect Neur, 2022, 17(12): 1101-1117.

1. 胡素. 情绪面孔启动情绪的神经基础: 来自大脑诱发和自发神经活动模式的证据. 杭州: 浙江师范大学, 2023.
2. 王静, 田小霖, 王雄飞, 等. 基于立体定向脑电图记录恐惧情绪的神经网络研究. 中国现代神经疾病杂志, 2023, 23(3): 189-195.
3. Zidda F, Andoh J, Pohlack S, et al. Default mode network connectivity of fear-and anxiety-related cue and context conditioning. NeuroImage, 2018, 165: 190-199.
4. Stark R, Schienle A, Walter B, et al. Hemodynamic responses to fear and disgust-inducing pictures: an fMRI study. Int J Psychophysiol, 2003, 50(3): 225-234.
5. Landová E, Rádlová S, Pidnebesna A, et al. Toward a reliable detection of arachnophobia: subjective, behavioral, and neurophysiological measures of fear response. Front Psychiatry, 2023, 14: 1196785.
6. Kroes M C W, Dunsmoor J E, Hakimi M, et al. Patients with dorsolateral prefrontal cortex lesions are capable of discriminatory threat learning but appear impaired in cognitive regulation of subjective fear. Soc Cogn Affect Neur, 2019, 14(6): 601-612.
7. Dilger S, Straube T, Mentzel H J, et al. Brain activation to phobia-related pictures in spider phobic humans: an event-related functional magnetic resonance imaging study. Neurosci Lett, 2003, 348(1): 29-32.
8. Schupp H T, Stockburger J, Codispoti M, et al. Stimulus novelty and emotion perception: the near absence of habituation in the visual cortex. Neuroreport, 2006, 17(4): 365-369.
9. Ding R, Li P, Wang W, et al. Emotion processing by ERP combined with development and plasticity. Neural Plast, 2017, 2017: 5282670.
10. Schupp H T, Kirmse U M. Case-by-case: Emotional stimulus significance and the modulation of the EPN and LPP. Psychophysiology, 2021, 58(4): e13766.
11. Aldunate N, López V, Bosman C A. Early influence of affective context on emotion perception: EPN or Early-N400?. Front Neurosci, 2018, 12: 413585.
12. Van Strien J W, Van der Peijl M K. Enhanced early visual processing in response to snake and trypophobic stimuli. BMC psychology, 2018, 6: 1-8.
13. Langeslag S J E, Van Strien J W. Early visual processing of snakes and angry faces: an ERP study. Brain Res, 2018, 1678: 297-303.
14. Zhou F, Zhao W, Qi Z, et al. A distributed fMRI-based signature for the subjective experience of fear. Nat Commun, 2021, 12(1): 6643.
15. Stefanescu M R, Endres R J, Hilbert K, et al. Networks of phobic fear: Functional connectivity shifts in two subtypes of specific phobia. Neurosci Lett, 2018, 662: 167-172.
16. Hassan M, Wendling F. Electroencephalography source connectivity: aiming for high resolution of brain networks in time and space. IEEE Signal Proc Mag, 2018, 35(3): 81-96.
17. Grech R, Cassar T, Muscat J, et al. Review on solving the inverse problem in EEG source analysis. J Neuroeng Rehabil, 2008, 5: 1-33.
18. Trettin M, Dvoák J, Hilke M, et al. Neuronal response to high negative affective stimuli in major depressive disorder: An fMRI study. J Affect Disorders, 2022, 298: 239-247.
19. 尹宁, 张家皓, 王海力, 等. 磁刺激穴位调节负性情绪的脑电溯源和脑网络研究. 电工技术学报, 2021, 36(4): 756-764.
20. Thom N, Knight J, Dishman R, et al. Emotional scenes elicit more pronounced self-reported emotional experience and greater EPN and LPP modulation when compared to emotional faces. Cogn Affect Behav Ne, 2014, 14: 849-860.
21. Zhang Y, Chen S, Deng Z, et al. Benefits of implicit regulation of instructed fear: Evidence from neuroimaging and functional connectivity. Front Neurosci, 2020, 14: 514367.
22. Milad M R, Wright C I, Orr S P, et al. Recall of fear extinction in humans activates the ventromedial prefrontal cortex and hippocampus in concert. Biol Psychiat, 2007, 62(5): 446-454.
23. Kummar A S, Correia H, Fujiyama H. A brief review of the EEG literature on mindfulness and fear extinction and its potential implications for posttraumatic stress symptoms (PTSS). Brain Sci, 2019, 9(10): 258.
24. Maffei A, Coccaro A, Jaspers-Fayer F, et al. EEG alpha band functional connectivity reveals distinct cortical dynamics for overt and covert emotional face processing. Sci Rep, 2023, 13(1): 9951.
25. Bacigalupo F, Luck S J. Alpha-band EEG suppression as a neural marker of sustained attentional engagement to conditioned threat stimuli. Soc Cogn Affect Neur, 2022, 17(12): 1101-1117.

Journal of Biomedical Engineering

Neural mechanisms of fear responses to emotional stimuli: a preliminary study combining early posterior negativity and electroencephalogram source network analysis

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