Impairment of decision making and disruption of synchrony between basolateral amygdala and anterior cingulate cortex in the maternally separated rat

Bing Cao, Jun Wang, Xu Zhang, Xiangwei Yang, David Chun Hei Poon, Beth Jelfs, Rosa H.M. Chan, Justin Che Yuen Wu, Ying Li

Research output: Contribution to journalArticlepeer-review

15 Citations (Scopus)

Abstract

There is considerable evidence to suggest early life experiences, such as maternal separation (MS), play a role in the prevalence of emotional dysregulation and cognitive impairment. At the same time, optimal decision making requires functional integrity between the amygdala and anterior cingulate cortex (ACC), and any dysfunction of this system is believed to induce decision-making deficits. However, the impact of MS on decision-making behavior and the underlying neurophysiological mechanisms have not been thoroughly studied. As such, we consider the impact of MS on the emotional and cognitive functions of rats by employing the open-field test, elevated plus-maze test, and rat gambling task (RGT). Using multi-channel recordings from freely behaving rats, we assessed the effects of MS on the large scale synchrony between the basolateral amygdala (BLA) and the ACC; while also characterizing the relationship between neural spiking activity and the ongoing oscillations in theta frequency band across the BLA and ACC. The results indicated that the MS rats demonstrated anxiety-like behavior. While the RGT showed a decrease in the percentage of good decision-makers, and an increase in the percentage of poor decision-makers. Electrophysiological data revealed an increase in the total power in the theta band of the LFP in the BLA and a decrease in theta power in the ACC in MS rats. MS was also found to disrupt the spike-field coherence of the ACC single unit spiking activity to the ongoing theta oscillations in the BLA and interrupt the synchrony in the BLA-ACC pathway. We provide specific evidence that MS leads to decision-making deficits that are accompanied by alteration of the theta band LFP in the BLA-ACC circuitries and disruption of the neural network integrity. These observations may help revise fundamental notions regarding neurophysiological biomarkers to treat cognitive impairment induced by early life stress.

Original languageEnglish
Pages (from-to)74-85
Number of pages12
JournalNeurobiology of Learning and Memory
Volume136
DOIs
Publication statusPublished - 1 Dec 2016
Externally publishedYes

Bibliographical note

Funding Information:
This work was supported by the Research Grants Council of Hong Kong [grant number 11166116 , 11100914 , 160811 , 160812 , and 160713 , 11101315 to Y. Li], the Innovation and Technology Support Programme [ ITS/300/15 to Y. Li], the Health and Medical Research Fund of Hong Kong [ 01122006 to Y. Li], City University of Hong Kong Neuroscience Research Infrastructure Grant [ 9610211 to Y. Li], and City University of Hong Kong Centre for Biosystems, Neuroscience, and Nanotechnology Grant [to S. Pang and Y. Li].

Publisher Copyright:
© 2016 Elsevier Inc.

Keywords

  • Anterior cingulate cortex
  • Anxiety
  • Basolateral amygdala
  • Decision-making
  • Maternal separation
  • Theta synchronization

ASJC Scopus subject areas

  • Experimental and Cognitive Psychology
  • Cognitive Neuroscience
  • Behavioral Neuroscience

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