Stress increases GABAergic neurotransmission in CRF neurons of the central amygdala and bed nucleus stria terminalis

Partridge, John G.; Forcelli, Patrick A.; Luo, Ruixi; Cashdan, Jonah M.; Schulkin, Jay; Valentino, Rita J.; Vicini, Stefano

doi:10.1016/j.neuropharm.2016.03.029

Cited by 71 publications

(76 citation statements)

References 77 publications

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“…However, its influence on the distribution of sIPSC amplitude was significant in these cells, reflecting increases in the fraction of sIPSCs with larger amplitudes. Actually, several earlier studies have found that acute stress enhanced the efflux of GABA in BA [29] and its neighboring central amygdala [30]. Thus, acute stress also recruits the inhibitory network in BA.…”

Section: Discussionmentioning

confidence: 97%

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

Song

Zhang²,

Wang³

et al. 2017

Mol Brain

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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.Electronic supplementary materialThe online version of this article (doi:10.1186/s13041-016-0283-6) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 97%

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

Song

Zhang²,

Wang³

et al. 2017

Mol Brain

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“…Rouwette et al suggest that changes of CRF1 and CRF2 receptors expression in the CeAmy could underlie neuropathic pain [22]. A very recent paper demonstrated that chronic unpredictable stress alters the GABA neurotransmission between amygdala CRF neurons and inhibits CeAmy output to BNST [13]. It is plausible that persistent pain causes similar changes in CeAmy output that lead to inhibition of descending pain modulation and more specifically to inhibition of LC activity.…”

Section: Discussionmentioning

confidence: 99%

“…The CeAmy is a key element in descending inhibition of pain and is essential for robust SIA [11]. The projections of the CeAmy target the bed nucleus of stria terminalis (BNST) and several brainstem nuclei, including the LC [12, 13]. There is general agreement that CeAmy CRF neurons do not affect baseline sensory thresholds but their role in pain is not clear.…”

Section: Introductionmentioning

confidence: 99%

Contribution of amygdala CRF neurons to chronic pain

Andreoli

Marketkar

Dimitrov

2017

Experimental Neurology

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We investigated the role of amygdala corticotropin-releasing factor (CRF) neurons in the perturbations of descending pain inhibition caused by neuropathic pain. Forced swim increased the tail-flick response latency in uninjured mice, a phenomenon known as stress-induced analgesia (SIA) but did not change the tail-flick response latency in mice with neuropathic pain caused by sciatic nerve constriction. Neuropathic pain also increased the expression of CRF in the central amygdala (CeAmy) and ΔFosB in the dorsal horn of the spinal cord. Next, we injected the CeAmy of CRF-cre mice with cre activated AAV-DREADD (Designer Receptors Exclusively Activated by Designer Drugs) vectors. Activation of CRF neurons by DREADD/Gq did not affect the impaired SIA but inhibition of CRF neurons by DREADD/Gi restored SIA and decreased allodynia in mice with neuropathic pain. The possible downstream circuitry involved in the regulation of SIA was investigated by combined injections of retrograde cre-virus (CAV2-cre) into the locus ceruleus (LC) and cre activated AAV-diphtheria toxin (AAV-FLEX-DTX) virus into the CeAmy. The viral injections were followed by a sciatic nerve constriction ipsilateral or contralateral to the injections. Ablation of amygdala projections to the LC on the side of injury but not on the opposite side, completely restored SIA, decreased allodynia and decreased ΔFosB expression in the spinal cord in mice with neuropathic pain. The possible lateralization of SIA impairment to the side of injury was confirmed by an experiment in which unilateral inhibition of the LC decreased SIA even in uninjured mice. The current view in the field of pain research attributes the process of pain chronification to abnormal functioning of descending pain inhibition. Our results demonstrate that the continuous activity of CRF neurons brought about by persistent pain leads to impaired SIA, which is a symptom of dysregulation of descending pain inhibition. Therefore, an over-activation of amygdala CRF neurons is very likely an important contributing factor for pain chronification.

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“…The peptide can be synthesized and stored at specific GABAergic and glutamatergic synapses (Cain et al, 1991; Valentino et al, 2001a; Valentino et al, 2001b), and is usually co-released with classical neurotransmitters (Partridge et al, 2016) in response to neuronal firing to modulate their synaptic effects (Rainnie et al, 1992; Yu and Shinnick-Gallagher, 1998). The CRF system can produce a variety of region-, cell type- and synapse-specific effects depending on the distribution of its signaling elements within local and regional circuits (Henckens et al, 2016a).…”

Section: Introductionmentioning

confidence: 99%

CRF modulates glutamate transmission in the central amygdala of naïve and ethanol-dependent rats

et al. 2017

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Corticotropin-releasing factor (CRF) signaling in the central nucleus of the amygdala (CeA) is hypothesized to drive the development of alcohol dependence, as it regulates ethanol intake and several anxiogenic behaviors linked to withdrawal. Excitatory glutamatergic neurotransmission contributes to alcohol reinforcement, tolerance and dependence. Therefore, in this study we used in vitro slice electrophysiology to investigate the effects of CRF and its receptor subtype (CRF1 and CRF2) antagonists on both evoked and spontaneous action potential-independent glutamatergic transmission in the CeA of naive and ethanol-dependent Sprague-Dawley rats. We found that CRF (25–200 nM) concentration-dependently diminished evoked compound excitatory postsynaptic potentials (EPSPs), but increased miniature excitatory postsynaptic current (mEPSC) frequencies similarly in CeA neurons of both naïve and ethanol-dependent rats, indicating reduced evoked glutamatergic responses and enhanced vesicular glutamate release, respectively. This CRF-induced vesicular glutamate release was prevented by the CRF1/2 antagonist (Astressin B) and the CRF1 antagonist (R121919), but not by the CRF2 antagonist (Astressin 2B). Similarly, CRF’s effects on evoked glutamatergic responses were completely blocked by CRF1 antagonism, but only slightly decreased in the presence of the CRF2 antagonist. Moreover, CRF1 antagonism reveals a tonic facilitation of vesicular glutamate, whereas the CRF2 antagonism revealed a tonic inhibition of vesicular glutamate release. Collectively our data show that CRF primarily acts at presynaptic CRF1 to produce opposite effects on CeA evoked and spontaneous glutamatergic release and that the CRF system modulates CeA glutamatergic synapses throughout the development of alcohol dependence.

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Stress increases GABAergic neurotransmission in CRF neurons of the central amygdala and bed nucleus stria terminalis

Cited by 71 publications

References 77 publications

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

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

Contribution of amygdala CRF neurons to chronic pain

CRF modulates glutamate transmission in the central amygdala of naïve and ethanol-dependent rats

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