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Thalamic Stimulation Improves Postictal Cortical Arousal and Behavior

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Thalamic Stimulation Improves Postictal Cortical Arousal and Behavior Research Articles: Behavioral/Cognitive Thalamic stimulation improves postictal cortical arousal and behavior https://doi.org/10.1523/JNEUROSCI.1370-20.2020 Cite as: J. Neurosci 2020; 10.1523/JNEUROSCI.1370-20.2020 Received: 31 May 2020 Revised: 9 August 2020 Accepted: 10 August 2020 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2020 the authors 1 Thalamic stimulation improves postictal cortical arousal and behavior 2 Abbreviated title: Thalamic stimulation improves postictal arousal 3 Jingwen Xu1,6, Maria Milagros Galardi1, Brian Pok1, Kishan K. Patel1, Charlie W. Zhao1, John P. 4 Andrews1, Shobhit Singla1, Cian P. McCafferty1, Li Feng1, Eric. T. Musonza1, Adam. J. 5 Kundishora1,3, Abhijeet Gummadavelli1,3, Jason L. Gerrard3, Mark Laubach4, Nicholas D. 6 Schiff5, Hal Blumenfeld1,2,3 7 8 Departments of 1Neurology, 2Neuroscience, 3Neurosurgery, Yale University School of Medicine, 9 New Haven, CT, USA 10 4 Department of Biology, American University, Washington, DC, USA 11 5Department of Neurology, Weill-Cornell Medical College, New York, NY, USA 12 6Department of Neurology, Qilu Hospital, Cheeloo College of Medicine, Shandong University, 13 Jinan, Shandong, 250012, China 14 15 Correspondence to: Hal Blumenfeld, MD, PhD 16 Yale Depts. Neurology, Neuroscience, Neurosurgery 17 333 Cedar Street, New Haven, CT 06520-8018 18 Tel: 203 785-3865 Fax: 203 737-2538 19 Email: [email protected] 20 21 Key words: epilepsy, thalamus, deep brain stimulation (DBS), consciousness, generalized tonic- 22 clonic seizures, sleep 23 24 Number of pages: 39 25 Number of figures: 6, color figures: 2, tables: 0. 26 Number of words in the Abstract: 250, Introduction: 650, Discussion: 1247. 27 Xu et al. 2 28 Conflicts of Interest: the authors declare no competing non-financial/financial interests. 29 30 Acknowledgements: 31 We thank Dr. Kate Christison-Lagay for artwork in Figure 1A. This work was supported by NIH 32 R01 NS066974, R01 NS096088, the Mark Loughridge and Michele Williams Foundation, and 33 the Betsy and Jonathan Blattmachr family (HB) and a China Scholarship Council fellowship 34 (JX). 35 36 37 2 Xu et al. 3 38 Abstract 39 Objective: The postictal state following seizures is characterized by impaired consciousness and 40 has a major negative impact on individuals with epilepsy. Previous work in disorders of 41 consciousness including the postictal state suggests that bilateral deep brain stimulation (DBS) of 42 the thalamic intralaminar central lateral nuclei (CL) may improve level of arousal. Methods: We 43 tested the effects of postictal thalamic CL DBS in a rat model of secondarily generalized seizures 44 elicited by electrical hippocampal stimulation. Thalamic CL DBS was delivered at 100 Hz 45 during the postictal period in 21 female rats while measuring cortical electrophysiology and 46 behavior. Results: The postictal period was characterized by frontal cortical slow waves, like 47 other states of depressed consciousness. In addition, rats exhibited severely impaired responses 48 on two different behavioral tasks in the postictal state. Thalamic CL stimulation prevented 49 postictal cortical slow wave activity but produced only modest behavioral improvement on a 50 spontaneous licking sucrose reward task. We therefore also tested responses using a lever press 51 shock escape/avoidance (E/A) task. Rats achieved high success rates responding to the sound 52 warning on the E/A task even during natural slow wave sleep but were severely impaired in the 53 postictal state. Unlike the spontaneous licking task, thalamic CL DBS during the E/A task 54 produced a marked improvement in behavior, with significant increases in lever press shock 55 avoidance with DBS compared to sham controls. Interpretation: These findings support the 56 idea that DBS of subcortical arousal structures may be a novel therapeutic strategy benefitting 57 patients with medically and surgically refractory epilepsy. 58 Significance Statement 59 The postictal state following seizures is characterized by impaired consciousness and has a major 60 negative impact on individuals with epilepsy. For the first time, we developed two behavioral 3 Xu et al. 4 61 tasks and demonstrate that bilateral deep brain stimulation (DBS) of the thalamic intralaminar 62 central lateral nuclei (CL) decreased cortical slow activity and improved task performance in the 63 postictal period. Because pre-clinical task performance studies are crucial to explore the 64 effectiveness and safety of DBS treatment, our work is clinically relevant as it could support and 65 help set the foundations for a human neurostimulation trial to improve postictal responsiveness 66 in patients with medically and surgically refractory epilepsy. 67 4 Xu et al. 5 68 Introduction 69 The postictal state that follows epileptic seizures comprises a broad spectrum of disturbances 70 including behavior, motor function, cognitive, autonomic and psychological changes and can last 71 from minutes to days (Helmstaedter et al., 1994; Fisher and Schachter, 2000; Todd, 2005; Remi 72 and Noachtar, 2010; Schmidt and Noachtar, 2010; Theodore, 2010; Werhahn, 2010; Carlsson et 73 al., 2011). Postictal symptoms can be more debilitating on patients with epilepsy than the ictal 74 events. It has been shown that postictal cognitive and behavioral impairment have a significant 75 correlation with depression in adults with epilepsy (Josephson et al., 2016). Postictal 76 consciousness impairment in school-age children is a cause of decreased attention that negatively 77 impacts their education (Elliott et al., 2005). Postictal phenomena prevented over 50% of 78 affected children from returning to their normal activities of childhood (MacEachern et al., 2017). 79 Furthermore, longer postictal generalized EEG suppression duration has been associated with 80 risk of sudden unexpected death in epilepsy (SUDEP) (Hesdorffer and Tomson, 2013; Seyal et 81 al., 2013; Rugg-Gunn et al., 2016; Tomson et al., 2016). Importantly, postictal immobility 82 duration is associated with respiratory dysfunction (Kuo et al., 2016) which may be a causal 83 factor in SUDEP (Ryvlin et al., 2013; Zhan et al., 2014). Given all of these findings, reversing 84 impaired arousal and postictal immobility may reduce SUDEP risk and could significantly 85 improve the quality of life of people with epilepsy. 86 In recent years, neurostimulation of subcortical regions has emerged as a promising 87 therapy for the treatment of refractory seizures (Fisher and Velasco, 2014; Heck et al., 2014; 88 Benedetti-Isaac et al., 2015; Klinger and Mittal, 2018). The mechanism by which consciousness 89 is lost during and after temporal lobe seizures has been consolidated in the “network inhibition 90 hypothesis” – inhibition of subcortical arousal structures may result in cortical states resembling 5 Xu et al. 6 91 deep sleep or coma during and after seizures (Norden and Blumenfeld, 2002; Blumenfeld, 2012). 92 Thus, therapeutic activation of these subcortical arousal structures could attenuate the loss of 93 consciousness experienced in focal seizures. 94 Specifically, the intralaminar thalamic nuclei receive input from the brainstem arousal 95 system and have been shown to play an important role in awareness (Van der Werf et al., 2002; 96 Schiff et al., 2007; Schiff et al., 2013; Baker et al., 2016). These nuclei contain matrix neurons 97 that project to the cortex and synchronize activity in neural networks that drive cognitive 98 functions (Jones, 2009). Previous studies have demonstrated benefits of stimulating the thalamic 99 intralaminar central lateral nucleus (CL) in restoring arousal. In asleep rats, central thalamic 100 stimulation produced widespread activation of the forebrain (Liu et al., 2015). Deep brain 101 stimulation (DBS) within CL and the medial dorsal thalamic tegmental tract in nonhuman 102 primates produced a robust modulation of performance and arousal, (Baker et al., 2016). In a 103 landmark human study, thalamic CL DBS improved arousal and functional behavioral 104 performance for a patient in the minimally conscious state (Schiff et al., 2007). More recently, 105 CL stimulation was found to effectively restore arousal and wake-like neural processing in 106 anesthetized macaques (Redinbaugh et al., 2020). Previous studies in a rodent model of limbic 107 seizures have also shown that bilateral CL DBS improved cortical electrophysiological arousal 108 and spontaneous locomotor behaviors during deep anesthesia, sleep and the postictal period 109 (Gummadavelli et al., 2015a; Kundishora et al., 2017). However, whether purposeful goal- 110 oriented behavior can be restored in the postical period through CL DBS remains to be 111 determined and is crucial for translational value to human therapy. 112 Here, our aim is to further investigate CL DBS effects in the postictal period using a 113 rodent model of secondarily generalized limbic seizures. We tested two different behavioral 6 Xu et al. 7 114 tasks for the first time in an animal model of postictal unconsciousness; a positive reinforcement 115 spontaneous-licking sucrose reward task and a negative reinforcement lever-press escape- 116 avoidance task. By assessing electrophysiological
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