Acute stress enhances the glutamatergic transmission onto basoamygdala neurons embedded in distinct microcircuits

Molecular Brain, Jan 2017

Amygdala activation is known to be critical for the processing of stressful events in brain. Recent studies have shown that the projection neurons (PNs) in amygdala, although architecturally intermingled, are integrated into distinct microcircuits and thus play divergent roles in amygdala-related behaviors. It remains unknown how stress regulates the individual amygdala PNs embedded in distinct microcircuits. Here, by using retrograde tracing and electrophysiological recording in in vitro slices, we explored the modulation of acute immobilization stress (AIS) on the basoamygdala (BA) PNs projecting either to medial prefrontal cortex (mPFC) or elsewhere, which we designated as BA-mPFC and non-BA-mPFC PNs respectively. The results showed that in the control mice, both the excitatory and inhibitory postsynaptic currents (sEPSCs/sIPSCs) were comparable between these two subsets of BA PNs. The influences of AIS on sEPSCs and sIPSCs were overall similar between the two neuronal populations. It markedly increased the sEPSCs amplitude but left unaltered their frequency as well as the sIPSCs amplitude and frequency. Despite this, several differences emerged between the effects of AIS on the distribution of sEPSCs/sIPSCs frequency in these two groups of BA PNs. Similar changes were also observed in the sEPSCs/sIPSCs of the two PN populations from mice experiencing forced swimming stress. Their intrinsic excitability, on the other hand, was nearly unaltered following AIS. Our results thus suggest that acute stress recruit both BA-mPFC and non-BA-mPFC PNs mainly through enhancing the glutamatergic transmission they receive.

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Acute stress enhances the glutamatergic transmission onto basoamygdala neurons embedded in distinct microcircuits

Song et al. Molecular Brain Acute stress enhances the glutamatergic transmission onto basoamygdala neurons embedded in distinct microcircuits Chen Song 0 1 Wen-Hua Zhang 1 Xue-Hui Wang 1 Jun-Yu Zhang 1 Xiao-Li Tian 0 Xiao-Ping Yin Bing-Xing P n 0 1 0 College of Life Science , 330031 Nanchang , China 1 Laboratory of Fear and Anxiety Disorders, Institute of Life Science , 330031 Nanchang , China Amygdala activation is known to be critical for the processing of stressful events in brain. Recent studies have shown that the projection neurons (PNs) in amygdala, although architecturally intermingled, are integrated into distinct microcircuits and thus play divergent roles in amygdala-related behaviors. It remains unknown how stress regulates the individual amygdala PNs embedded in distinct microcircuits. Here, by using retrograde tracing and electrophysiological recording in in vitro slices, we explored the modulation of acute immobilization stress (AIS) on the basoamygdala (BA) PNs projecting either to medial prefrontal cortex (mPFC) or elsewhere, which we designated as BA-mPFC and non-BA-mPFC PNs respectively. The results showed that in the control mice, both the excitatory and inhibitory postsynaptic currents (sEPSCs/sIPSCs) were comparable between these two subsets of BA PNs. The influences of AIS on sEPSCs and sIPSCs were overall similar between the two neuronal populations. It markedly increased the sEPSCs amplitude but left unaltered their frequency as well as the sIPSCs amplitude and frequency. Despite this, several differences emerged between the effects of AIS on the distribution of sEPSCs/sIPSCs frequency in these two groups of BA PNs. Similar changes were also observed in the sEPSCs/sIPSCs of the two PN populations from mice experiencing forced swimming stress. Their intrinsic excitability, on the other hand, was nearly unaltered following AIS. Our results thus suggest that acute stress recruit both BA-mPFC and non-BA-mPFC PNs mainly through enhancing the glutamatergic transmission they receive. Amygdala; Acute stress; Intrinsic excitability; Medial prefrontal cortex; Spontaneous postsynaptic current - Background Effectively coping with the stressful events in daily life is critical for the survival of organisms [1]. It has been known for decades that the stress coping system is evolutionally conservative in brain across species ranging from rodents to primates and to humans [2]. Amygdala is one of the kernel parts of this system and responsible for receiving and integrating different modes of information from sensory cortex and thalamus and passing them down to the executive nuclei in the hypothalamus or brainstem to elicit a spectrum of stress responses [3], including increased startle reactivity, heightened autonomic tone and activation of neuroendocrine axes [4, 5]. As such, amygdala activation has been generally regarded as an important neuronal correlate for stress processing inside the brain [6–9]. As commonly known, amygdala is a complex composed of more than ten sub-nuclei [10]. Among them, the basal part of amygdala (BA) acts to bridge the information flow from the lateral amygdala, the main reception of sensory information entering amygdala to the central amygdala, the main exit of information processed inside amygdala [11]. It also accounts for the intercommunication between amygdala and many other regions including prefrontal cortex, hippocampus and ventral striatum [10]. One prominent architectural feature which distinguishes BA from its neighboring regions is that the projection neurons (PNs) in this region, unlike © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. those in cerebral cortex or hippocampus exhibiting clear laminar and columnar organization, are extensively intermingled [12]. Despite this, increasing evidence in recent years has demonstrated that the intermingled BA neurons are integrated into distinct functional circuits and thus have divergent or even opposing roles in the processing of emotionally salient events in amygdala [13–16]. For example, optogenetic activation of the BA terminals projecting to nucleus accumbens (NAc) drives positive reinforcement while BA projections to the central amygdala are related with negative valence [14]. Given the critical role of amygdala activation in brain processing of stress [9], it remains unknown how stress exposure affects the BA PNs integrated into distinct functional circ (...truncated)


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Chen Song, Wen-Hua Zhang, Xue-Hui Wang, Jun-Yu Zhang, Xiao-Li Tian, Xiao-Ping Yin, Bing-Xing Pan. Acute stress enhances the glutamatergic transmission onto basoamygdala neurons embedded in distinct microcircuits, Molecular Brain, 2017, pp. 3, 10, DOI: 10.1186/s13041-016-0283-6