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
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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
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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)