Synaptic plasticity and synchrony in the anterior cingulate cortex circuitry : A neural network approach to causality of chronic visceral pain and associated cognitive deficits

Research output: Chapters, Conference Papers, Creative and Literary Works (RGC: 12, 32, 41, 45)12_Chapter in an edited book (Author)peer-review

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Author(s)

Detail(s)

Original languageEnglish
Title of host publicationSystems Neuroscience
EditorsAlbert Cheung-Hoi Yu, Lina Li
PublisherSpringer International Publishing AG
Pages219-245
ISBN (Electronic)9783319945934
ISBN (Print)9783319945910
Publication statusPublished - 2018

Publication series

NameAdvances in Neurobiology
Volume21
ISSN (Print)2190-5215
ISSN (Electronic)2190-5223

Abstract

Human brain imaging studies have demonstrated the importance of cortical neuronal networks in the perception of pain in patients with functional bowel disease such as irritable bowel syndrome (IBS).

Studies have identified an enhanced response in the anterior cingulate cortex (ACC) to colorectal distension in viscerally hypersensitive (VH) rats. Electrophysiological recordings show long-lasting potentiation of local field potential (LFP) in the medial thalamus (MT)-ACC synapses in VH rats. Theta burst stimulation in the MT reliably induced long-term potentiation (LTP) in the MT-ACC pathway in normal rats, but was occluded in the VH state. Further, repeated tetanization of MT increased ACC neuronal activity and visceral pain responses of normal rats, mimicking VH rats. These data provide conclusive evidence that chronic visceral pain is associated with alterations of synaptic plasticity in the ACC circuitry. The ACC synaptic strengthening may engage signal transduction pathways that are in common with those activated by electrical stimulation, and serve as an attractive cellular model of functional visceral pain.

Evidences have shown that most patients with IBS have psychiatric comorbidity. Using rat gambling task (RGT), we discovered an impairment of decision-making behavior in VH rats. Electrophysiological study showed a reduction of LTP in the basolateral amygdala (BLA)-ACC synapses in VH rats. Multiple-electrode array recordings of local field potential (LFP) in freely behaving rats revealed that chronic visceral pain led to disruption of ACC spike timing and BLA local theta oscillation. Finally, cross-correlation analysis revealed that VH was associated with suppressed synchronization of theta oscillation between the BLA and ACC, indicating reduced neuronal communications between these two regions. These data suggest that functional disturbances in BLA-ACC neural circuitry may be relevant causes for the deficits in decision-making in chronic pain state.

The viscero-sensation is a faculty of perception that does not depend upon any outward sense, but acts to influence the elicited behavioral response. Clinically, vagus nerve stimulation (VNS) has shown several beneficial effects for mood enhancement. Our recent study characterized that VNS facilitates decision-making and unveiled several important roles for VNS in regulating LFP and spike phases, as well as enhancing spike-phase coherence between key brain areas involved in cognitive performance.

It is conceivable that the visceral pain experience may be better explained as a biopsychosocial model of pain and reflected in a matrix of neuronal structures. Understanding of desynchrony in the ACC network and cognitive deficits is likely to provide exciting and powerful future treatment for chronic visceral pain related debilitating mood, anxiety, and cognitive disorders.

Research Area(s)

  • Anterior cingulate cortex, Basolateral amygdala, Cognitive deficit, Decision-making, N-methyl-D-aspartate (NMDA) receptor, Phase-locking, Spike field coherence, Synaptic plasticity, Theta synchronization, Visceral hypersensitivity

Citation Format(s)

Synaptic plasticity and synchrony in the anterior cingulate cortex circuitry: A neural network approach to causality of chronic visceral pain and associated cognitive deficits. / Li, Ying.
Systems Neuroscience. ed. / Albert Cheung-Hoi Yu; Lina Li. Springer International Publishing AG, 2018. p. 219-245 (Advances in Neurobiology; Vol. 21).

Research output: Chapters, Conference Papers, Creative and Literary Works (RGC: 12, 32, 41, 45)12_Chapter in an edited book (Author)peer-review