Impairment of decision making and disruption of synchrony between basolateral amygdala and anterior cingulate cortex in the maternally separated rat.
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.
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China. Electronic address: bingcao4-c@my.cityu.edu.hk.
Bing
B
Cao
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China. Electronic address: juwang9-c@my.cityu.edu.hk.
Jun
J
Wang
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China. Electronic address: xuzhang1637@gmail.com.
Xu
X
Zhang
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China. Electronic address: xianyang@cityu.edu.hk.
Xiangwei
X
Yang
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China. Electronic address: davidpoonhku@gmail.com.
David Chun-Hei
DC
Poon
Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China; Department of Electronic Engineering, City University of Hong Kong, Kowloon, Hong Kong, China. Electronic address: beth.jelfs@cityu.edu.hk.
Beth
B
Jelfs
Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China; Department of Electronic Engineering, City University of Hong Kong, Kowloon, Hong Kong, China. Electronic address: rosachan@cityu.edu.hk.
Rosa H M
RH
Chan
Department of Medicine and Therapeutics, The Chinese University of Hong Kong, Hong Kong, China. Electronic address: justinwu@cuhk.edu.hk.
Justin Che-Yuen
JC
Wu
Department of Biomedical Sciences, City University of Hong Kong, Hong Kong, China; Centre for Biosystems, Neuroscience, and Nanotechnology, City University of Hong Kong, Hong Kong, China; School of Veterinary Medicine, City University of Hong Kong, Kowloon, Hong Kong, China. Electronic address: yingli@cityu.edu.hk.
Ying
Y
Li
D000818:Animals; D001007:Anxiety / Q000209:etiology / Q000503:physiopathology*; D066272:Basolateral Nuclear Complex / Q000503:physiopathology*; D001522:Behavior, Animal / Q000502:physiology; D060825:Cognitive Dysfunction / Q000209:etiology / Q000503:physiopathology*; D003657:Decision Making / Q000502:physiology*; D004195:Disease Models, Animal; D058407:Electroencephalography Phase Synchronization / Q000502:physiology*; D005260:Female; D006179:Gyrus Cinguli / Q000503:physiopathology*; D008297:Male; D008426:Maternal Deprivation; D018782:Maze Learning / Q000502:physiology; D011247:Pregnancy; D051381:Rats; D017207:Rats, Sprague-Dawley; D013826:Theta Rhythm / Q000502:physiology*
Anterior cingulate cortex; Anxiety; Basolateral amygdala; Decision-making; Maternal separation; Theta synchronization