Trigeminal neuropathy causes hypomyelination in the anterior cingulate cortex, disrupts the synchrony of neural circuitry, and impairs decision-making in male rats,Journal of Neuroscience Research

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Trigeminal neuropathy causes hypomyelination in the anterior cingulate cortex, disrupts the synchrony of neural circuitry, and impairs decision-making in male rats
Journal of Neuroscience Research ( IF 2.9 ) Pub Date : 2021-07-29 , DOI: 10.1002/jnr.24903
Suresh K Murugappan ₁ , Mahadi Hasan _{1,

2} , Zhuogui Lei _{1,

2} , Zafar Iqbal _{1,

2,

3} , Aruna S Ramkrishnan _{1,

2} , Heung Y Wong _{1,

2,

3} , Ying Li _{1,

2,

3,

4}

Affiliation

Infraorbital nerve-chronic constriction injury (ION-CCI) has become the most popular chronic trigeminal neuropathic pain (TNP) injury animal model which causes prolonged mechanical allodynia. Accumulative evidence suggests that TNP interferes with cognitive functions, however the underlying mechanisms are not known. The aim of this study was to investigate decision-making performance as well as synaptic and large-scale neural synchronized alterations in the spinal trigeminal nucleus (SpV) circuitry and anterior cingulate cortex (ACC) neural circuitry in male rats with TNP. Rat gambling task showed that ION-CCI led to decrease the proportion of good decision makers and increase the proportion of poor decision makers. Electrophysiological recordings showed long-lasting synaptic potentiation of local field potential in the trigeminal ganglia-SpV caudalis (SpVc) synapses in TNP rats. In this study, TNP led to disruption of ACC spike timing and basolateral amygdala (BLA) theta oscillation associated with suppressed synchronization of theta oscillation between the BLA and ACC, indicating reduced neuronal communications. Myelination is critical for information flow between brain regions, and myelin plasticity is an important feature for learning. Neural activity in the cortical regions impacts myelination by regulating oligodendrocyte (OL) proliferation, differentiation, and myelin formation. We characterized newly formed oligodendrocyte progenitor cells, and mature OLs are reduced in TNP and are associated with reduced myelin strength in the ACC region. The functional disturbances in the BLA-ACC neural circuitry is pathologically associated with the myelin defects in the ACC region which may be relevant causes for the deficits in decision-making in chronic TNP state.

中文翻译：

三叉神经病变导致前扣带回皮层髓鞘发育不全，破坏神经回路的同步性，并损害雄性大鼠的决策能力

眶下神经慢性收缩损伤（ION-CCI）已成为最流行的慢性三叉神经痛（TNP）损伤动物模型，可导致长时间的机械异常性疼痛。越来越多的证据表明，TNP 会干扰认知功能，但其潜在机制尚不清楚。本研究的目的是研究 TNP 雄性大鼠脊髓三叉神经核 (SpV) 电路和前扣带皮层 (ACC) 神经电路的决策性能以及突触和大规模神经同步改变。大鼠赌博任务表明，ION-CCI导致良好决策者比例降低，而不良决策者比例增加。电生理记录显示 TNP 大鼠三叉神经节-SpV 尾部 (SpVc) 突触中局部场电位的长期突触增强。在这项研究中，TNP 导致 ACC 尖峰时间和基底外侧杏仁核 (BLA) theta 振荡的中断，这与 BLA 和 ACC 之间的 theta 振荡同步抑制相关，表明神经元通讯减少。髓鞘形成对于大脑区域之间的信息流动至关重要，而髓鞘可塑性是学习的重要特征。皮质区域的神经活动通过调节少突胶质细胞 (OL) 的增殖、分化和髓鞘形成来影响髓鞘形成。我们对新形成的少突胶质祖细胞进行了表征，成熟的 OL 在 TNP 中减少，并与 ACC 区域的髓鞘强度降低有关。

更新日期：2021-07-29

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