Electro-clinical correlation for “Chapeau de gendarme” sign and gamma oscillations_Journal of Epilepsy

Authors：

LU Hongjuan ¹ , ZHANG Wei ² , LONG Qiting ² , ZHANG Cuirong ³ , SHANG Li ³ ,  LIU Xingzhou ² ,  SUN Wei ¹

1. Department of Neurology, Xuanwu Hospital Capital Medical University, Beijing 100053, China;
2. Department of Neurology, Beijing Tsinghua Changgung Hospital, School of Clinical Medicine, Tsinghua University, Beijing 102218, China;
3. Epilepsy Center, Shanghai Deji Hospital, Qingdao University, Shanghai 200126, China;

Corresponding author：

LIU Xingzhou, Email: sinclairliu@sina.cn; SUN Wei, Email: bmusunnyw@163.com

Keywords：

Chapeau de gendarme; Agranulo-dysgranular insulo-cingulate cortices; γ frequency oscillations; Electro-clinical correlation

DOI：

10.7507/2096-0247.202209002

Video：

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Objective The time relationship between seizure semiology and epileptic discharges during focal epileptic seizures is a crucial predictor for the localization of epileptogenic zone. Low voltage fast activities (LVFA), especially gamma band oscillations, are confirmed to play a central role in ictogenesis and semiology production. In the present study, we focus on the “electro-clinical correlation” between LVFA in agranulo-dysgranular insulo-cingulate cortices and the sign of “Chapeau de gendarme (CDG)” via detailed analysis of ictal video-stereoencephalography (video-SEEG) of focal epileptic seizures. Methods We retrospectively analyzed the ictal video-SEEG of the 7 cases in which CDG signs were presented in habitual seizures and intracerebral electrodes were co-implanted in agranulo-dysgranular insular and cingulate cortices. We calculate the latency of LVFA in each of cortical regions of interest, agranulo-dygranular insular cortex, agranulo-dysgranular cingulate cortex, and the latency of CDG signs via visual and spectral analysis of the ictal SEEG. Moreover, Pearson correlation analysis and linear regression were used to test the time relationship between gamma band oscillations in agranulo-dysgranular insulo-cingulate cortices and generation of CDG signs. Results The co-activation of LVFA occurred in agranulo-dysgranular insulo-cingulate cortices always preceded the appearance of CDG sign in all of the 69 seizures. The LVFA were confirmed as gamma band oscillations via spectral analysis of SEEG. A linear relationship between the latencies of CDG signs and the latencies of co-activation of agranulo-dysgranular insulo-cingulate cortices in gamma band was furth confirmed by Pearson correlation analysis and linear regression. Conclusions There is a causal relationship between the involvement of agranulo-dysgranular insulo-cingulate cortices and the generation of CDG sign, and thus the CDG sign could be view as semiological marker of activation of emotional insulo-cingulate cortex in focal epilepsy.

Citation： LU Hongjuan, ZHANG Wei, LONG Qiting, ZHANG Cuirong, SHANG Li, LIU Xingzhou, SUN Wei. Electro-clinical correlation for “Chapeau de gendarme” sign and gamma oscillations. Journal of Epilepsy, 2022, 8(6): 509-516. doi: 10.7507/2096-0247.202209002 Copy

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3.	Cebeci D, Arhan E, Hirfanoglu T, et al. Ictal pouting ('Chapeau de gendarme') in three pediatric cases with cortical dysplasia. Eur J Paediatr Neurol, 2020, 26: 82-88.
4.	Hayakawa I, Kubota M. Ictal pouting: kabuki visage or chapeau de gendarme? Practical Neurology, 2018, 18(5): 410-412.
5.	Lu H, Zhang W, Long Q, et al. A semiological marker of emotional insulo-cingulate network activation in epileptic human brain. Epilepsy Behav, 2021, 120: 107970.
6.	Chauvel P, Rheims S, McGonigal A, et al. French guidelines on stereoelectroencephalography (SEEG): Editorial comment. Neurophysiologie Clinique, 2018, 48(1): 1-3.
7.	Chauvel P, McGonigal A. Emergence of semiology in epileptic seizures. Epilepsy Behav, 2014, 38: 94-103.
8.	McGonigal A. Contribution of Seizure Semiology to Diagnosis of Anatomo-electrical Localisation of Epilepsy. University of Glasgow, 2015.
9.	de Curtis M, Gnatkovsky V. Reevaluating the mechanisms of focal ictogenesis: The role of low-voltage fast activity. Epilepsia, 2009, 50(12): 2514-2525.
10.	Vignal J P, Maillard L, McGonigal A, et al. The dreamy state: hallucinations of autobiographic memory evoked by temporal lobe stimulations and seizures. Brain, 2006, 130(1): 88-99.
11.	Bartolomei F, Barbeau EJ, Nguyen T, et al. Rhinalhippocampal interactions during déjà vu. Clin Neurophysiol, 2012, 123: 489-95.
12.	Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, et al. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron, 2012, 76: 804-812.
13.	Aupy J, Noviawaty I, Krishnan B, et al, Gonzalez-Martinez J, Najm I, Chauvel P. Insulo-opercular cortex generates oroalimentary automatisms in temporal seizures. Epilepsia. 2018, 59(3): 583-594.
14.	Zilles K, Amunts K. Architecture of the cerebral cortex. The Human Nervous System, 2012, 15: 836-895.
15.	Barbas H. General cortical and special prefrontal connections: principles from structure to function. Annu Rev Neurosci, 2015, 38: 269-289.
16.	Craig AD. How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci, 2009, 10(1): 59-70.
17.	Morel A, Gallay MN, Baechler A, et al. The human insula: Architectonic organization and postmortem MRI registration. Neuroscience, 2013, 236: 117-135.
18.	Amunts K, Lenzen M, Friederici A D, et al. Broca's region: novel organizational principles and multiple receptor mapping. PLoS Biol, 2010, 8(9): 325-329.
19.	Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science, 2004, 304: 1926-1929.
20.	Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci, 2001, 2(10): 704-716.
21.	Salinas E, Sejnowski TJ. Correlated neuronal activity and the flow of neural information. Nature Rev Neurosci, 2001, 2(5): 539-550.
22.	Siegel M, Donner TH, Engel AK. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci, 2012, 13(2): 121-134.
23.	Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci, 1995, 18: 555-586.
24.	Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci, 2007, 8(1): 45-56.
25.	Bauer M, Oostenveld R, Peeters M, et al. Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci, 2006, 26(2): 490-501.
26.	Bragin A, Jando G, Nadasdy Z, et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci, 1995, 15(1 Pt. 1): 47-60.
27.	Brosch M, Budinger E, Scheich H. Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol, 2002, 87(6): 2715-2725.
28.	Castelo-Branco M, Neuenschwander S, Singer W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J Neurosci, 1998, 18(16): 6395-63410.
29.	Neuenschwander S, Singer W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature, 1996, 379(6567): 728-732.
30.	Pesaran B, Pezaris JS, Sahani M, et al. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci, 2002, 5(8): 805-811.
31.	Bosman CA, Lansink CS, Pennartz CM. Functions of gamma-band synchronization in cognition: from single circuits to functional diversity across cortical and subcortical systems. Eur J Neurosci, 2014, 39(11): 1982-1999.
32.	Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci, 2009, 32: 209-224.
33.	Kepecs A, Fishell G. Interneuron cell types are fit to function. Nature, 2014, 505(7483): 318-326.
34.	Lytton WW, Sejnowski TJ. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol, 1991, 66(3): 1059-1079.
35.	Buzsáki G, Wang XJ. Mechanisms of gamma oscillations. Annu Rev Neurosci, 2012, 35: 203-225.
36.	Nieuwenhuys R. The insular cortex: a review. Progress in Brain Research, 2012, 195: 123-163.
37.	Caruana F, Jezzini A, Sbriscia-Fioretti B, et al. Emotional and social behavior elicited by electrical stimulation of the insula in the macaque monkey. Current Biology, 2011, 21: 195-199.
38.	Vogt BA. Cingulate cortex in the three limbic subsystems. Handb Clin Neurol, 2019, 166: 39-51.
39.	Vogt BA, Pandya DN. Cingulate cortex of the rhesus monkey: II cortical afferents. J Comp Neurol, 1987, 262(2): 271-289.
40.	Vogt BA, Palomero-Gallagher N. Cingulate cortex In: Mai JK, Paxinos G, Editors. The human nervous system. Academic Press, 2012: 943-987.
41.	Rolls ET. The cingulate cortex and limbic systems for action, emotion, and memory. Handb Clin Neurol, 2019, 166: 23-37.
42.	Bartoli E, Conner CR, Kadipasaoglu CM, et al. Temporal dynamics of human frontal and cingulate neural activity during conflict and cognitive control. Cereb Cortex, 2018, 28(11): 3842-3856.
43.	Luo Q, Mitchell D, Cheng X, et al. Visual awareness, emotion, and gamma band synchronization. Cerebral Cortex, 2009, 19(8): 1896-1904.
44.	Vogt BA. Midcingulate cortex: structure, connections, homologies, functions and diseases. J Chem Neuroanat, 2016, 74: 28-46.
45.	Morecraft RJ, Van Hoesen GW. Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res Bull, 1998, 45(2): 209-232.
46.	Yokiyama O, Nakayama Y, Hoshi E. Area-and band-specific representations of hand movements by local field potentials in caudal cingulate motor area and supplementary motor area of monkeys. J Neurophysiol, 2016, 115: 1556-1576.
47.	Voloh B, Valiante TA, Everling S, et al. Theta-gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts. Proc Natl Acad Sci USA, 2015, 112(27): 8457-8462.
48.	Ham T, Leff A, de Boissezon X, et al. Cognitive control and the salience network: an investigation of error processing and effective connectivity. J Neurosci, 2013, 33: 7091-7098.
49.	Taylor KS, Seminowicz DA, Davis KD. Two systems of resting state connectivity between the insula and cingulate cortex. Hum Brain Mapp, 2009, 30: 2731-2745.
50.	Chand GB, Dhamala M. Interactions between the anterior cingulate-insula network and the fronto-parietal network during perceptual decision-making. NeuroImage, 2017, 152: 381-389.
51.	Grinenko O, Li J, Mosher JC, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain, 2018, 141(1): 117-131.
52.	Lévesque M, Shiri Z, Chen LY, et al. High-frequency oscillations and mesial temporal lobe epilepsy. Neuroscience Letters, 2018, 667: 66-74.
53.	Morecraft R J, Tanji J. Cingulofrontal Interactions and the cingulate motor areas. In:Vogt BA, editor. Cingulate neurobiology and disease. Oxford University Press, 2009: 113-144.
54.	Allman JM, Tetreault NA, Hakeem AY, et al. The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct, 2010, 214(5-6): 495-517.
55.	Hodge RD, Miller JA, Novotny M, et al. Transcriptomic evidence that von Economo neurons are regionally specialized extratelencephalic-projecting excitatory neurons. Nat Commun, 2020, 11(1): 1172.

1. Bonini F, McGonigal A, Trébuchon A, et al. Frontal lobe seizures: From clinical semiology to localization. Epilepsia (Copenhagen), 2014, 55(2): 264-277.
2. Souirti Z, Landre E, Mellerio C, et al. Neural network underlying ictal pouting ("chapeau de gendarme") in frontal lobe epilepsy. Epilepsy Behav, 2014, 37: 249-257.
3. Cebeci D, Arhan E, Hirfanoglu T, et al. Ictal pouting ('Chapeau de gendarme') in three pediatric cases with cortical dysplasia. Eur J Paediatr Neurol, 2020, 26: 82-88.
4. Hayakawa I, Kubota M. Ictal pouting: kabuki visage or chapeau de gendarme? Practical Neurology, 2018, 18(5): 410-412.
5. Lu H, Zhang W, Long Q, et al. A semiological marker of emotional insulo-cingulate network activation in epileptic human brain. Epilepsy Behav, 2021, 120: 107970.
6. Chauvel P, Rheims S, McGonigal A, et al. French guidelines on stereoelectroencephalography (SEEG): Editorial comment. Neurophysiologie Clinique, 2018, 48(1): 1-3.
7. Chauvel P, McGonigal A. Emergence of semiology in epileptic seizures. Epilepsy Behav, 2014, 38: 94-103.
8. McGonigal A. Contribution of Seizure Semiology to Diagnosis of Anatomo-electrical Localisation of Epilepsy. University of Glasgow, 2015.
9. de Curtis M, Gnatkovsky V. Reevaluating the mechanisms of focal ictogenesis: The role of low-voltage fast activity. Epilepsia, 2009, 50(12): 2514-2525.
10. Vignal J P, Maillard L, McGonigal A, et al. The dreamy state: hallucinations of autobiographic memory evoked by temporal lobe stimulations and seizures. Brain, 2006, 130(1): 88-99.
11. Bartolomei F, Barbeau EJ, Nguyen T, et al. Rhinalhippocampal interactions during déjà vu. Clin Neurophysiol, 2012, 123: 489-95.
12. Sotres-Bayon F, Sierra-Mercado D, Pardilla-Delgado E, et al. Gating of fear in prelimbic cortex by hippocampal and amygdala inputs. Neuron, 2012, 76: 804-812.
13. Aupy J, Noviawaty I, Krishnan B, et al, Gonzalez-Martinez J, Najm I, Chauvel P. Insulo-opercular cortex generates oroalimentary automatisms in temporal seizures. Epilepsia. 2018, 59(3): 583-594.
14. Zilles K, Amunts K. Architecture of the cerebral cortex. The Human Nervous System, 2012, 15: 836-895.
15. Barbas H. General cortical and special prefrontal connections: principles from structure to function. Annu Rev Neurosci, 2015, 38: 269-289.
16. Craig AD. How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci, 2009, 10(1): 59-70.
17. Morel A, Gallay MN, Baechler A, et al. The human insula: Architectonic organization and postmortem MRI registration. Neuroscience, 2013, 236: 117-135.
18. Amunts K, Lenzen M, Friederici A D, et al. Broca's region: novel organizational principles and multiple receptor mapping. PLoS Biol, 2010, 8(9): 325-329.
19. Buzsáki G, Draguhn A. Neuronal oscillations in cortical networks. Science, 2004, 304: 1926-1929.
20. Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci, 2001, 2(10): 704-716.
21. Salinas E, Sejnowski TJ. Correlated neuronal activity and the flow of neural information. Nature Rev Neurosci, 2001, 2(5): 539-550.
22. Siegel M, Donner TH, Engel AK. Spectral fingerprints of large-scale neuronal interactions. Nat Rev Neurosci, 2012, 13(2): 121-134.
23. Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci, 1995, 18: 555-586.
24. Bartos M, Vida I, Jonas P. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci, 2007, 8(1): 45-56.
25. Bauer M, Oostenveld R, Peeters M, et al. Tactile spatial attention enhances gamma-band activity in somatosensory cortex and reduces low-frequency activity in parieto-occipital areas. J Neurosci, 2006, 26(2): 490-501.
26. Bragin A, Jando G, Nadasdy Z, et al. Gamma (40–100 Hz) oscillation in the hippocampus of the behaving rat. J Neurosci, 1995, 15(1 Pt. 1): 47-60.
27. Brosch M, Budinger E, Scheich H. Stimulus-related gamma oscillations in primate auditory cortex. J Neurophysiol, 2002, 87(6): 2715-2725.
28. Castelo-Branco M, Neuenschwander S, Singer W. Synchronization of visual responses between the cortex, lateral geniculate nucleus, and retina in the anesthetized cat. J Neurosci, 1998, 18(16): 6395-63410.
29. Neuenschwander S, Singer W. Long-range synchronization of oscillatory light responses in the cat retina and lateral geniculate nucleus. Nature, 1996, 379(6567): 728-732.
30. Pesaran B, Pezaris JS, Sahani M, et al. Temporal structure in neuronal activity during working memory in macaque parietal cortex. Nat Neurosci, 2002, 5(8): 805-811.
31. Bosman CA, Lansink CS, Pennartz CM. Functions of gamma-band synchronization in cognition: from single circuits to functional diversity across cortical and subcortical systems. Eur J Neurosci, 2014, 39(11): 1982-1999.
32. Fries P. Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu Rev Neurosci, 2009, 32: 209-224.
33. Kepecs A, Fishell G. Interneuron cell types are fit to function. Nature, 2014, 505(7483): 318-326.
34. Lytton WW, Sejnowski TJ. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J Neurophysiol, 1991, 66(3): 1059-1079.
35. Buzsáki G, Wang XJ. Mechanisms of gamma oscillations. Annu Rev Neurosci, 2012, 35: 203-225.
36. Nieuwenhuys R. The insular cortex: a review. Progress in Brain Research, 2012, 195: 123-163.
37. Caruana F, Jezzini A, Sbriscia-Fioretti B, et al. Emotional and social behavior elicited by electrical stimulation of the insula in the macaque monkey. Current Biology, 2011, 21: 195-199.
38. Vogt BA. Cingulate cortex in the three limbic subsystems. Handb Clin Neurol, 2019, 166: 39-51.
39. Vogt BA, Pandya DN. Cingulate cortex of the rhesus monkey: II cortical afferents. J Comp Neurol, 1987, 262(2): 271-289.
40. Vogt BA, Palomero-Gallagher N. Cingulate cortex In: Mai JK, Paxinos G, Editors. The human nervous system. Academic Press, 2012: 943-987.
41. Rolls ET. The cingulate cortex and limbic systems for action, emotion, and memory. Handb Clin Neurol, 2019, 166: 23-37.
42. Bartoli E, Conner CR, Kadipasaoglu CM, et al. Temporal dynamics of human frontal and cingulate neural activity during conflict and cognitive control. Cereb Cortex, 2018, 28(11): 3842-3856.
43. Luo Q, Mitchell D, Cheng X, et al. Visual awareness, emotion, and gamma band synchronization. Cerebral Cortex, 2009, 19(8): 1896-1904.
44. Vogt BA. Midcingulate cortex: structure, connections, homologies, functions and diseases. J Chem Neuroanat, 2016, 74: 28-46.
45. Morecraft RJ, Van Hoesen GW. Convergence of limbic input to the cingulate motor cortex in the rhesus monkey. Brain Res Bull, 1998, 45(2): 209-232.
46. Yokiyama O, Nakayama Y, Hoshi E. Area-and band-specific representations of hand movements by local field potentials in caudal cingulate motor area and supplementary motor area of monkeys. J Neurophysiol, 2016, 115: 1556-1576.
47. Voloh B, Valiante TA, Everling S, et al. Theta-gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts. Proc Natl Acad Sci USA, 2015, 112(27): 8457-8462.
48. Ham T, Leff A, de Boissezon X, et al. Cognitive control and the salience network: an investigation of error processing and effective connectivity. J Neurosci, 2013, 33: 7091-7098.
49. Taylor KS, Seminowicz DA, Davis KD. Two systems of resting state connectivity between the insula and cingulate cortex. Hum Brain Mapp, 2009, 30: 2731-2745.
50. Chand GB, Dhamala M. Interactions between the anterior cingulate-insula network and the fronto-parietal network during perceptual decision-making. NeuroImage, 2017, 152: 381-389.
51. Grinenko O, Li J, Mosher JC, et al. A fingerprint of the epileptogenic zone in human epilepsies. Brain, 2018, 141(1): 117-131.
52. Lévesque M, Shiri Z, Chen LY, et al. High-frequency oscillations and mesial temporal lobe epilepsy. Neuroscience Letters, 2018, 667: 66-74.
53. Morecraft R J, Tanji J. Cingulofrontal Interactions and the cingulate motor areas. In:Vogt BA, editor. Cingulate neurobiology and disease. Oxford University Press, 2009: 113-144.
54. Allman JM, Tetreault NA, Hakeem AY, et al. The von Economo neurons in frontoinsular and anterior cingulate cortex in great apes and humans. Brain Struct Funct, 2010, 214(5-6): 495-517.
55. Hodge RD, Miller JA, Novotny M, et al. Transcriptomic evidence that von Economo neurons are regionally specialized extratelencephalic-projecting excitatory neurons. Nat Commun, 2020, 11(1): 1172.

Journal of Epilepsy

Electro-clinical correlation for “Chapeau de gendarme” sign and gamma oscillations

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