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

Research output: Journal Publications and ReviewsRGC 21 - Publication in refereed journalpeer-review

3 Scopus Citations
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Author(s)

  • Mahadi Hasan
  • Aruna S. Ramkrishnan
  • Heung Y. Wong

Detail(s)

Original languageEnglish
Pages (from-to)2721-2742
Number of pages22
Journal / PublicationJournal of Neuroscience Research
Volume99
Issue number10
Online published29 Jul 2021
Publication statusPublished - Oct 2021

Link(s)

Abstract

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.

Research Area(s)

  • anterior cingulate cortex, brain network oscillations, decision-making, myelin plasticity, spike-field phase locking, trigeminal neuropathic pain

Citation Format(s)

Trigeminal neuropathy causes hypomyelination in the anterior cingulate cortex, disrupts the synchrony of neural circuitry, and impairs decision-making in male rats. / Murugappan, Suresh K.; Hasan, Mahadi; Lei, Zhuogui et al.
In: Journal of Neuroscience Research, Vol. 99, No. 10, 10.2021, p. 2721-2742.

Research output: Journal Publications and ReviewsRGC 21 - Publication in refereed journalpeer-review

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