Deep Brain Stimulation of the Anterior Nuclei of the Thalamus Relieves Basal Ganglia Dysfunction in Monkeys with Temporal Lobe Epilepsy

Overview

Journal CNS Neurosci Ther

Specialties Neurology
Pharmacology

Date 2020 Oct 21

PMID 33085171

Citations 12

Authors

Tingting Du

Yingchuan Chen

Lin Shi

Defeng Liu

Yuye Liu

Tianshuo Yuan

Xin Zhang

Guanyu Zhu

Jianguo Zhang

Affiliations

Soon will be listed here.

Abstract

Aims: Deep brain stimulation of the anterior nuclei of the thalamus (ANT-DBS) is effective in temporal lobe epilepsy (TLE). Previous studies have shown that the basal ganglia are involved in seizure propagation in TLE, but the effects of ANT-DBS on the basal ganglia have not been clarified.

Methods: ANT-DBS was applied to monkeys with kainic acid-induced TLE using a robot-assisted system. Behavior was monitored continuously. Immunofluorescence analysis and Western blotting were used to estimate protein expression levels in the basal ganglia and the effects of ANT stimulation.

Results: The seizure frequency decreased after ANT-DBS. D1 and D2 receptor levels in the putamen and caudate were significantly higher in the ANT-DBS group than in the epilepsy (EP) model. Neuronal loss and apoptosis were less severe in the ANT-DBS group. Glutamate receptor 1 (GluR1) in the nucleus accumbens (NAc) shell and globus pallidus internus (GPi) increased in the EP group but decreased after ANT-DBS. γ-Aminobutyric acid receptor A (GABA -R) decreased and glutamate decarboxylase 67 (GAD67) increased in the GPi of the EP group, whereas the reverse tendencies were observed after ANT-DBS.

Conclusion: ANT-DBS exerts neuroprotective effects on the caudate and putamen, enhances D1 and D2 receptor expression, and downregulates GPi overactivation, which enhanced the antiepileptic function of the basal ganglia.

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References

Barone P, Parashos S, Palma V, Marin C, Campanella G, Chase T . Dopamine D1 receptor modulation of pilocarpine-induced convulsions. Neuroscience. 1990; 34(1):209-17. DOI: 10.1016/0306-4522(90)90314-t. View

Yang A, Shi L, Li L, Li J, Jiang Y, Meng D . Potential Protective Effects of Chronic Anterior Thalamic Nucleus Stimulation on Hippocampal Neurons in Epileptic Monkeys. Brain Stimul. 2015; 8(6):1049-57. DOI: 10.1016/j.brs.2015.07.041. View

McNamara J, Galloway M, Rigsbee L, Shin C . Evidence implicating substantia nigra in regulation of kindled seizure threshold. J Neurosci. 1984; 4(9):2410-7. PMC: 6564806. View

Ito M, Doya K . Multiple representations and algorithms for reinforcement learning in the cortico-basal ganglia circuit. Curr Opin Neurobiol. 2011; 21(3):368-73. DOI: 10.1016/j.conb.2011.04.001. View

Friedman D, Aggleton J, Saunders R . Comparison of hippocampal, amygdala, and perirhinal projections to the nucleus accumbens: combined anterograde and retrograde tracing study in the Macaque brain. J Comp Neurol. 2002; 450(4):345-65. DOI: 10.1002/cne.10336. View

Meredith G, Agolia R, Arts M, Groenewegen H, Zahm D . Morphological differences between projection neurons of the core and shell in the nucleus accumbens of the rat. Neuroscience. 1992; 50(1):149-62. DOI: 10.1016/0306-4522(92)90389-j. View

Kowski A, Voges J, Heinze H, Oltmanns F, Holtkamp M, Schmitt F . Nucleus accumbens stimulation in partial epilepsy--a randomized controlled case series. Epilepsia. 2015; 56(6):e78-82. DOI: 10.1111/epi.12999. View

Nishi A, Kuroiwa M, Shuto T . Mechanisms for the modulation of dopamine d(1) receptor signaling in striatal neurons. Front Neuroanat. 2011; 5:43. PMC: 3140648. DOI: 10.3389/fnana.2011.00043. View

DeCarli C, Hatta J, Fazilat S, Gaillard W, Theodore W . Extratemporal atrophy in patients with complex partial seizures of left temporal origin. Ann Neurol. 1998; 43(1):41-5. DOI: 10.1002/ana.410430110. View

10.

Dinner D, Neme S, Nair D, Montgomery Jr E, Baker K, Rezai A . EEG and evoked potential recording from the subthalamic nucleus for deep brain stimulation of intractable epilepsy. Clin Neurophysiol. 2002; 113(9):1391-402. DOI: 10.1016/s1388-2457(02)00185-2. View

11.

Akkal D, Dum R, Strick P . Supplementary motor area and presupplementary motor area: targets of basal ganglia and cerebellar output. J Neurosci. 2007; 27(40):10659-73. PMC: 6672811. DOI: 10.1523/JNEUROSCI.3134-07.2007. View

12.

Zhu G, Chen Y, Du T, Liu D, Zhang X, Liu Y . The Accuracy and Feasibility of Robotic Assisted Lead Implantation in Nonhuman Primates. Neuromodulation. 2019; 22(4):441-450. DOI: 10.1111/ner.12951. View

13.

Fedi M, Berkovic S, Scheffer I, OKeefe G, Marini C, Mulligan R . Reduced striatal D1 receptor binding in autosomal dominant nocturnal frontal lobe epilepsy. Neurology. 2008; 71(11):795-8. DOI: 10.1212/01.wnl.0000316192.52731.77. View

14.

Xing L, McDonald H, Da Fonte D, Gutierrez-Villagomez J, Trudeau V . Dopamine D1 receptor activation regulates the expression of the estrogen synthesis gene aromatase B in radial glial cells. Front Neurosci. 2015; 9:310. PMC: 4557113. DOI: 10.3389/fnins.2015.00310. View

15.

Wichmann T, DeLong M . Deep Brain Stimulation for Movement Disorders of Basal Ganglia Origin: Restoring Function or Functionality?. Neurotherapeutics. 2016; 13(2):264-83. PMC: 4824026. DOI: 10.1007/s13311-016-0426-6. View

16.

Pulsipher D, Seidenberg M, Morton J, Geary E, Parrish J, Hermann B . MRI volume loss of subcortical structures in unilateral temporal lobe epilepsy. Epilepsy Behav. 2007; 11(3):442-9. PMC: 3680513. DOI: 10.1016/j.yebeh.2007.08.007. View

17.

Vesper J, Steinhoff B, Rona S, Wille C, Bilic S, Nikkhah G . Chronic high-frequency deep brain stimulation of the STN/SNr for progressive myoclonic epilepsy. Epilepsia. 2007; 48(10):1984-9. DOI: 10.1111/j.1528-1167.2007.01166.x. View

18.

Cavalheiro E, Bortolotto Z, Turski L . Microinjections of the gamma-aminobutyrate antagonist, bicuculline methiodide, into the caudate-putamen prevent amygdala-kindled seizures in rats. Brain Res. 1987; 411(2):370-2. DOI: 10.1016/0006-8993(87)91089-4. View

19.

Du T, Chen Y, Shi L, Liu D, Liu Y, Yuan T . Deep brain stimulation of the anterior nuclei of the thalamus relieves basal ganglia dysfunction in monkeys with temporal lobe epilepsy. CNS Neurosci Ther. 2020; 27(3):341-351. PMC: 7871793. DOI: 10.1111/cns.13462. View

20.

Benabid A, Koudsie A, Benazzouz A, Vercueil L, Fraix V, Chabardes S . Deep brain stimulation of the corpus luysi (subthalamic nucleus) and other targets in Parkinson's disease. Extension to new indications such as dystonia and epilepsy. J Neurol. 2001; 248 Suppl 3:III37-47. DOI: 10.1007/pl00007825. View