Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus
Many epileptic seizures (hereafter abbreviated as seizures) are characterized by overly synchronized oscillating activities in the thalamocortical system. Despite dense reciprocal innervation between cortex and thalamus, the exact role of thalamus in ictogenesis (e.g. as a passive associate, lenient...
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Elsevier
2025-09-01
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| Series: | Neurobiology of Disease |
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| Online Access: | http://www.sciencedirect.com/science/article/pii/S0969996125002098 |
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| author | Ping Chou Yi-Chen Lai Yen-Hsin Zheng Ya-Chin Yang Chung-Chin Kuo |
| author_facet | Ping Chou Yi-Chen Lai Yen-Hsin Zheng Ya-Chin Yang Chung-Chin Kuo |
| author_sort | Ping Chou |
| collection | DOAJ |
| description | Many epileptic seizures (hereafter abbreviated as seizures) are characterized by overly synchronized oscillating activities in the thalamocortical system. Despite dense reciprocal innervation between cortex and thalamus, the exact role of thalamus in ictogenesis (e.g. as a passive associate, lenient modulator, or indispensable controller) has been unsettled. We found that either electrical or chemical ictogenic stimulation of basolateral amygdala (BLA) induces augmentation of δ-frequency local field potential (LFP) oscillations in situ. In contrast, the thalamic mediodorsal nucleus (MD), which is reciprocally connected with BLA, responds with mixed θ-α and δ oscillations at first. MD may then be entrained more and more into the latter, leading to augmented δ oscillations as well as δ coherence in the thalamocortical system and maximal behavioral seizures. Inhibition of MD with topical tetrodotoxin dissipates the coherent δ augmentation and decreases multi-unit spikes in BLA and other telencephalic areas, suggesting critical involvement of MD in the inter-cortical communication and focal ictogenesis. Systemic application of proconvulsant pentylenentetrazol could induce interchanging periods of δ and θ-α augmentation in MD, at which periods concomitant electrical stimulation of BLA would be much more and less likely to induce seizures, respectively. The mechanism underlying thalamic δ entrainment in telencephalic ictogenesis and “θ-α antagonism” may involve local GABA-glutamate interactions and the requirement of cortical glutamatergic input for the generation of thalamic burst discharges (“relay bursts''). Thalamus thus assumes a critical control of the temporal pace and spatial scale of telencephalic oscillations, with a specific but well adaptable order of frequency and amplitude modulation. |
| format | Article |
| id | doaj-art-556b89a96c61476b82ed4446b212049c |
| institution | Kabale University |
| issn | 1095-953X |
| language | English |
| publishDate | 2025-09-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Neurobiology of Disease |
| spelling | doaj-art-556b89a96c61476b82ed4446b212049c2025-08-20T03:55:48ZengElsevierNeurobiology of Disease1095-953X2025-09-0121310699310.1016/j.nbd.2025.106993Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamusPing Chou0Yi-Chen Lai1Yen-Hsin Zheng2Ya-Chin Yang3Chung-Chin Kuo4Department of Physiology, National Taiwan University College of Medicine, Taipei, TaiwanDepartment of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanGraduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, TaiwanDepartment of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, Taiwan; Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Taoyuan, Taiwan; Healthy Aging Research Center, Chang Gung University, Taoyuan, Taiwan; Department of Psychiatry, Chang Gung Memorial Hospital, Linkou Medical Center, Taoyuan, Taiwan; Correspondence to: Ya-Chin Yang, Ph.D., Department of Biomedical Sciences, College of Medicine, Chang Gung University, 259 Wen-Hwa 1st Road, Kwei-Shan, Taoyuan 333, Taiwan.Department of Physiology, National Taiwan University College of Medicine, Taipei, Taiwan; Department of Neurology, National Taiwan University Hospital, Taipei, Taiwan; Correspondence to: Chung-Chin Kuo, M.D., Ph.D., Department of Physiology, National Taiwan University College of Medicine, 1 Jen-Ai Road, 1st Section, Taipei 100, Taiwan.Many epileptic seizures (hereafter abbreviated as seizures) are characterized by overly synchronized oscillating activities in the thalamocortical system. Despite dense reciprocal innervation between cortex and thalamus, the exact role of thalamus in ictogenesis (e.g. as a passive associate, lenient modulator, or indispensable controller) has been unsettled. We found that either electrical or chemical ictogenic stimulation of basolateral amygdala (BLA) induces augmentation of δ-frequency local field potential (LFP) oscillations in situ. In contrast, the thalamic mediodorsal nucleus (MD), which is reciprocally connected with BLA, responds with mixed θ-α and δ oscillations at first. MD may then be entrained more and more into the latter, leading to augmented δ oscillations as well as δ coherence in the thalamocortical system and maximal behavioral seizures. Inhibition of MD with topical tetrodotoxin dissipates the coherent δ augmentation and decreases multi-unit spikes in BLA and other telencephalic areas, suggesting critical involvement of MD in the inter-cortical communication and focal ictogenesis. Systemic application of proconvulsant pentylenentetrazol could induce interchanging periods of δ and θ-α augmentation in MD, at which periods concomitant electrical stimulation of BLA would be much more and less likely to induce seizures, respectively. The mechanism underlying thalamic δ entrainment in telencephalic ictogenesis and “θ-α antagonism” may involve local GABA-glutamate interactions and the requirement of cortical glutamatergic input for the generation of thalamic burst discharges (“relay bursts''). Thalamus thus assumes a critical control of the temporal pace and spatial scale of telencephalic oscillations, with a specific but well adaptable order of frequency and amplitude modulation.http://www.sciencedirect.com/science/article/pii/S0969996125002098Thalamocortical oscillationsIctogenesisDelta oscillationsTheta-alpha oscillationsGABA-glutamate interactionsDelta entrainment |
| spellingShingle | Ping Chou Yi-Chen Lai Yen-Hsin Zheng Ya-Chin Yang Chung-Chin Kuo Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus Neurobiology of Disease Thalamocortical oscillations Ictogenesis Delta oscillations Theta-alpha oscillations GABA-glutamate interactions Delta entrainment |
| title | Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus |
| title_full | Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus |
| title_fullStr | Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus |
| title_full_unstemmed | Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus |
| title_short | Frequency-coded spatiotemporal control of telencephalic ictal oscillations and inter-cortical coherence by thalamus |
| title_sort | frequency coded spatiotemporal control of telencephalic ictal oscillations and inter cortical coherence by thalamus |
| topic | Thalamocortical oscillations Ictogenesis Delta oscillations Theta-alpha oscillations GABA-glutamate interactions Delta entrainment |
| url | http://www.sciencedirect.com/science/article/pii/S0969996125002098 |
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