Pulvinar neuromodulation for seizure monitoring and network modulation in temporal plus epilepsy

Vakilna, Yash Shashank; Chaitanya, Ganne; Hafeez, Muhammad Ubaid; Ilyas, Adeel; Saranathan, Manojkumar; Gavvala, Jay R.; Tandon, Nitin; Pati, Shibani

doi:10.1002/acn3.51815

Cited by 7 publications

(3 citation statements)

References 17 publications

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“…The safety of this procedure has been already discussed in previous studies 9,20 . Most of the patients in this study were implanted in the pulvinar (88/121) because of the known connections of the medial pulvinar with the limbic structures, the insula, and the lateral temporal cortex 7 and because this structure is emerging as a possible site for DBS implantation [21][22][23][24] . Moreover, the pulvinar is easily accessible when it is necessary to explore Heschl's cortex, in the process of defining language lateralization during the pre-surgical evaluation.…”

Section: Methodsmentioning

confidence: 99%

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

Biagioni,

Fratello,

Garnier

et al. 2024

Preprint

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Introduction: Addressing drug-resistant epilepsy poses a significant clinical hurdle, particularly when conventional resective surgery is not feasible. Deep brain stimulation (DBS) emerges as a potential therapeutic avenue for such cases. To shed light on the thalamo-cortical epileptogenic networks and refine prognostic indicators and treatments, we conducted an exhaustive examination of interictal data from thalamic stereoelectroencephalography (SEEG) recordings in a substantial patient cohort (n=121). Our investigation delved into thalamo-cortical connectivity, interictal hyperexcitability biomarkers, and their associations with clinical parameters during both rest and non-rapid eye movement (NREM) sleep states. Methodology: We conducted an observational study retrospectively gathering data from patients who underwent stereotactic-EEG with thalamic implantation as part of pre-surgical evaluation. Interictal recordings during rest and NREM sleep were analyzed to detect spikes and fast ripples automatically. Functional connectivity between the thalamus and other brain regions (involved or non-involved in the epileptogenic network) was examined using linear regression analysis (R2), while statistical evaluations assessed relationships between these measures, patient outcomes, and clinical variables. Results: Elevated rates of thalamic spikes and fast ripples during sleep were linked to unfavorable surgical outcomes (Engel class III/IV) compared to favorable outcomes (Engel class I/II). Thalamo-cortical functional connectivity analysis revealed heightened thalamic strength, particularly in the beta and gamma bands during sleep, among patients with poor surgical outcomes, especially with non-involved networks. Conversely, during rest, lower spike and fast ripple rates were observed in patients with longer epilepsy durations. Furthermore, thalamic strength values during resting state were diminished in patients with prolonged epilepsy durations and older age. Discussion: Our study uncovered heightened thalamic interictal activity and thalamo-cortical functional connectivity during sleep in patients with unfavorable surgical outcomes, within the largest cohort of patients with thalamic recordings documented. These findings inform pre-surgical assessments, aiding in identifying patients unsuitable for surgery and suggesting alternative interventions like DBS. Additionally, diminished thalamic activity and connectivity associated with epilepsy duration and age prompt speculation on the role of the thalamus as a pivotal hub in aging-related processes. Vigilance state-dependent insights from the thalamus underscore the necessity for comprehensive analyses to tailor stimulation protocols, facilitating a personalized therapeutic approach.

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Section: Methodsmentioning

confidence: 99%

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

Biagioni,

Fratello,

Garnier

et al. 2024

Preprint

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“…Similar to our prior studies ( Vakilna et al, 2023 ), Thalamus Optimized Multi-Atlas Segmentation (THOMAS) was utilized on the preoperative Fast Gray Matter Acquisition T1 Inversion Recovery (FGATIR) sequence to create the patient’s own CM nucleus segmentation ( Su et al, 2019 ; Vakilna et al, 2023 ). Post-implant CT and the FGATIR sequences were coregistered to the pre-implant T1 MRI using the Advanced Normalization Tools (ANTS).…”

Section: Methodsmentioning

confidence: 99%

Case report: Nocturnal low-frequency stimulation of the centromedian thalamic nucleus improves sleep quality and seizure control

Suresh,

Chaitanya,

Kachhvah

et al. 2024

Front. Hum. Neurosci.

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Sleep disturbances and drug-resistant seizures significantly impact people with idiopathic generalized epilepsy (IGE). Thalamic deep brain stimulation (DBS) offers potential treatment, but its effect on sleep and seizure control needs clarification. In this study, we combined wearable sleep monitoring with electroencephalogram (EEG) confirmation to investigate the impact of nocturnal centromedian nucleus (CM) DBS parameters in a patient with drug-resistant IGE. We found that high-frequency (125 Hz) CM stimulation during sleep severely disrupted sleep macro architecture and exacerbated seizures. Conversely, switching to low-frequency (10 Hz) stimulation enhanced both sleep quality and seizure control. This study underscores the critical need to personalize DBS settings, tailoring them to individual patients’ sleep patterns to maximize therapeutic benefits. While larger-scale trials are needed, our findings pave the way for patient-centric approaches to thalamic neuromodulation, offering a transformative path to improve treatment outcomes and quality of life for those with refractory epilepsy.

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“…This includes deep brain stimulation of the pulvinar, an emerging area of interest in functional neurosurgery for epilepsy, which could benefit from a deeper understanding of pulvinar connectivity and its implications for treatment outcomes (Kalamatianos et al 2023;Vakilna et al 2023;Wong et al 2023). Specifically, the medial (as opposed to the lateral) pulvinar is the desired target due to its connectivity to the medial temporal lobe.…”

Section: Neurochemical Correlates Of Pulvinar-cortical Topographical ...mentioning

confidence: 99%

The replication principle revisited: a shared functional organization between pulvinar-cortical and cortico-cortical connectivity and its structural and molecular imaging correlates

Basile,

Ielo,

Bonanno

et al. 2024

Preprint

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The pulvinar, the largest nucleus in the human thalamus, is a complex, highly interconnected structure. Through a dense, organized network of cortical and subcortical areas, it provides adequate cooperation between neural systems, which is crucial for multiple high-order functions such as perception, visuospatial attention, and emotional processing. Such a central role is made possible by a precise internal topographical organization, which is mirrored by anatomical connections as well as by the expression of neurochemical markers. While being traditionally subdivided into sub-nuclei, each characterized by distinct connectional and morphological features, recent studies in both primate and human brains have highlighted that this topographical organization only marginally aligns with the conventional histological subdivision. Instead, it has been delineated in the context of continuous gradients of cortical connections along the dorsoventral and mediolateral axes. While this multi-gradient organization has been extensively documented in primate models, it remains relatively underexplored in the human brain. The present work combines high-quality, multi-modal structural and functional imaging data with a recently published whole-brain, large-scale, positron emission tomography (PET) atlas detailing 19 neurotransmitters and receptors distributed across the human brain. By applying diffusion embedding analysis to tractography, functional connectivity, and receptor coexpression data, we identify and characterize multiple topographically organized gradients of structural connections, functional coactivation, and molecular binding patterns. We demonstrate that such gradients converge on a shared representation along the dorsoventral and mediolateral axes of the human pulvinar. This representation aligns with transitions in both structural and functional connectivity, spanning from lower-level to higher-order cortical regions. Moreover, it is paralleled by gradual changes in the expression of molecular markers associated with key neuromodulator systems, including serotoninergic, noradrenergic, dopaminergic, and opioid systems. We contend that our findings mark a significant stride towards a more comprehensive understanding of pulvinar anatomy and function, providing a nuanced characterization of its role in health and disease.

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Pulvinar neuromodulation for seizure monitoring and network modulation in temporal plus epilepsy

Cited by 7 publications

References 17 publications

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

Interictal waking and sleep electrophysiological properties of the thalamus in focal epilepsies

Case report: Nocturnal low-frequency stimulation of the centromedian thalamic nucleus improves sleep quality and seizure control

The replication principle revisited: a shared functional organization between pulvinar-cortical and cortico-cortical connectivity and its structural and molecular imaging correlates

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