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Ictal recruitment of anterior nucleus of thalamus in human focal epilepsy

Emilia Toth, Ganne Chaitanya, Diana Pizarro, Sachin S Kumar, Adeel Ilyas, Andrew Romeo, Kristen Riley, Ioannis Vlachos, Olivier David, Karthi Balasubramanian, Sandipan Pati
doi: https://doi.org/10.1101/788422
Emilia Toth
1Department of Neurology, University of Alabama at Birmingham, AL
2Epilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at Birmingham, AL
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Ganne Chaitanya
1Department of Neurology, University of Alabama at Birmingham, AL
2Epilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at Birmingham, AL
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Diana Pizarro
1Department of Neurology, University of Alabama at Birmingham, AL
2Epilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at Birmingham, AL
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Sachin S Kumar
4Centre for Computational Engineering and Networking (CEN), Amrita School of Engineering, Coimbatore, Amrita Vishwa Vidyapeetham, India
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Adeel Ilyas
2Epilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at Birmingham, AL
3Department of Neurosurgery, University of Alabama at Birmingham, AL
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Andrew Romeo
3Department of Neurosurgery, University of Alabama at Birmingham, AL
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Kristen Riley
3Department of Neurosurgery, University of Alabama at Birmingham, AL
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Ioannis Vlachos
5Department of Electrical and Computer Engineering, Aristotle University of Thessaloniki, Greece
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Olivier David
6Brain Stimulation and Systems Neuroscience, Grenoble Institute of Neuroscience
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Karthi Balasubramanian
7Department of Electronics and Communication Engineering, Amrita School of Engineering, Coimbatore, Amrita Vishwa Vidyapeetham, India
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Sandipan Pati
1Department of Neurology, University of Alabama at Birmingham, AL
2Epilepsy and Cognitive Neurophysiology Laboratory, University of Alabama at Birmingham, AL
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  • For correspondence: spati@uabmc.edu
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Abstract

The thalamic nuclei play diverse roles in the initiation, propagation, and termination of temporal lobe seizures. The role of the anterior nucleus of the thalamus (ANT) - a node that is integral to the limbic network is unclear. The objective of this study was to characterize temporal and - spectral patterns of ANT ictal recruitment in drug-resistant temporal lobe epilepsy (TLE). We hypothesized that seizures localized to the temporolimbic network are likely to recruit ANT, and the odds of recruitment were higher in seizures that had altered consciousness. Ten patients undergoing stereo-electroencephalography (SEEG) were recruited prospectively to record field potentials from the ANT. Using epileptogenicity index and line length, we computed the number of seizures that recruited the ANT (recruitment ratio), the recruitment latencies between the ANT and the epileptogenic zone (EZ), and latency of ANT recruitment to clinical manifestation for seventy-nine seizures. We observed that seizures localized to mesial temporal subregions (hippocampus, amygdala, anterior cingulate) have a higher predilection for ANT recruitment, and the recruitment was faster (ranged 5-12 secs) and preceded clinical onset for seizures that impaired consciousness. Seizures that recruited ANT lasted significantly longer (t=1.795, p=0.005). Recruitment latency was inversely correlated to seizure duration (r=-0.78, p=0.004). Electrical stimulation of the EZ induced seizures, in which early recruitment of ANT was confirmed. Stimulation of ANT did not induce a seizure. Finally, we tested the hypothesis that spectral and entropy-based features extracted from thalamic field potentials can distinguish its state of ictal recruitment from other interictal states (including awake, sleep). For this, we employed classification machine learning that discriminated thalamic ictal state from other interictal states with high accuracy (92.8%) and precision (93.1%). Among the features, the emergence of the theta rhythm (4-8 Hz) maximally discriminated the endogenous ictal state from other interictal states of vigilance. These results prompt a mechanistic role for the ANT in the early organization and sustaining of seizures, and the possibility to serve as a target for therapeutic closed-loop stimulation in TLE.

  • Abbreviations

    ASD
    Anti-seizure drugs
    DWT
    Discrete Wavelet Transfer
    EI
    Epileptogenecity Index
    ES
    Electrographic Seizures
    EZ
    Epileptogenic Zone
    FAS
    Focal Onset Aware Seizures
    FBTCS
    Focal to bilateral tonic-clonic seizures
    FIAS
    Focal onset seizures with impaired awareness
    HAAC
    Hippocampus, Amygdala, Anterior Cingulate complex
    LL
    Line Length
    MSE
    Multiscale Entropy
    RF
    Random Forest
    RKS
    Random Kitchen Sink
    RWE
    Relative Wavelet Energy
    SEEG
    stereo-electroencephalography
    TLE
    Temporal lobe epilepsy
    UEO
    Unequivocal electrographic onset
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    Posted October 01, 2019.
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    Ictal recruitment of anterior nucleus of thalamus in human focal epilepsy
    Emilia Toth, Ganne Chaitanya, Diana Pizarro, Sachin S Kumar, Adeel Ilyas, Andrew Romeo, Kristen Riley, Ioannis Vlachos, Olivier David, Karthi Balasubramanian, Sandipan Pati
    bioRxiv 788422; doi: https://doi.org/10.1101/788422
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    Ictal recruitment of anterior nucleus of thalamus in human focal epilepsy
    Emilia Toth, Ganne Chaitanya, Diana Pizarro, Sachin S Kumar, Adeel Ilyas, Andrew Romeo, Kristen Riley, Ioannis Vlachos, Olivier David, Karthi Balasubramanian, Sandipan Pati
    bioRxiv 788422; doi: https://doi.org/10.1101/788422

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