Corticotropin-releasing factor enhances inhibitory synaptic transmission to type III neurons in the bed nucleus of the stria terminalis

Nagano, Yuki; Kaneda, Katsuyuki; Maruyama, Chikashi; Ide, Soichiro; Kato, Fusao; Minami, Masabumi

doi:10.1016/j.neulet.2015.05.059

Cited by 15 publications

(8 citation statements)

References 21 publications

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“…Previous studies from our research group revealed that CRF preferentially depolarizes type II dlBNST neurons (Ide et al., ), whereas it increases inhibitory inputs to type III dlBNST neurons (Nagano et al., ). Furthermore, intra‐BNST injections of CRF enhance anxiety‐like behaviors in the EPM test (Sahuque et al., ).…”

Section: Discussionmentioning

confidence: 76%

“…BNST neurons can be electrophysiologically classified into three distinct cell types (types I–III) according to their responses to depolarizing and hyperpolarizing current injections (Hammack, Mania, & Rainnie, ). Our research group previously reported that CRF, which is an anxiogenic neuropeptide, increases neuronal excitability in type II dorsolateral BNST (dlBNST) neurons (Ide et al., ) whereas it enhances inhibitory inputs to type III dlBNST neurons (Nagano et al., ). Thus, the opposing effects of activation of LH/VTA‐projecting and CeA‐projecting BNST neurons on anxiety‐like behaviors may be due to differences in neuronal types in BNST neurons.…”

Section: Introductionmentioning

confidence: 99%

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Activation of the neural pathway from the dorsolateral bed nucleus of the stria terminalis to the central amygdala induces anxiety‐like behaviors

Yamauchi

Takahashi

Sugimura

et al. 2018

Eur J of Neuroscience

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The bed nucleus of the stria terminalis (BNST) and the central amygdala (CeA) comprise a forebrain unit that has been described as the “extended amygdala”. These two nuclei send dense projections to each other and have been implicated in the regulation of negative emotional states, including anxiety and fear. The present study employed an optogenetic technique to examine whether stimulation of CeA‐projecting dorsolateral BNST (dlBNST) neuron terminals would influence anxiety‐like behaviors in male Sprague‐Dawley rats. Photostimulation of CeA‐projecting dlBNST neuron terminals produced anxiogenic effects in an elevated plus maze test. This finding is inconsistent with previous reports showing that optogenetic stimulation of BNST neurons projecting to the lateral hypothalamus (LH) and ventral tegmental area (VTA) produces anxiolytic rather than anxiogenic effects. To address this issue, electrophysiological analyses were conducted to characterize dlBNST neurons projecting to the CeA, LH, and VTA. dlBNST neurons can be electrophysiologically classified into three distinct cell types (types I–III) according to their responses to depolarizing and hyperpolarizing current injections. Whole‐cell patch‐clamp recordings revealed that more than 60% of the CeA‐projecting dlBNST neurons were type II, whereas approximately 80% of the LH‐ and VTA‐projecting dlBNST neurons were type III. These electrophysiological results will help elucidate the mechanisms underlying the heterogeneity of BNST neurons during the regulation of anxiety‐like behaviors.

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Section: Discussionmentioning

confidence: 76%

Section: Introductionmentioning

confidence: 99%

Activation of the neural pathway from the dorsolateral bed nucleus of the stria terminalis to the central amygdala induces anxiety‐like behaviors

Yamauchi

Takahashi

Sugimura

et al. 2018

Eur J of Neuroscience

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“…Dumont & Williams () also demonstrated that noradrenaline increases the frequency of inhibitory postsynaptic currents (IPSC) in I h ‐negative (type III) vBNST neurons that project to the ventral tegmental area (VTA). Recently, our research group demonstrated that CRF increases inhibitory inputs to type III dlBNST neurons (Nagano et al ., ), in addition to its depolarizing effect on type II neurons. These findings, together with our previous histological study showing that most of BNST neurons express GAD67 mRNA (Kudo et al ., ), suggest the possible neuronal circuit where excitation of type II BNST neurons increases inhibitory inputs to type III BNST neurons that project to other brain regions, including the VTA.…”

Section: Discussionmentioning

confidence: 94%

Suppressive effects of morphine injected into the ventral bed nucleus of the stria terminalis on the affective, but not sensory, component of pain in rats

Maruyama

Deyama

Nagano

et al. 2017

Eur J of Neuroscience

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Pain is a complex experience with both sensory and affective components. Clinical and preclinical studies have shown that the affective component of pain can be reduced by doses of morphine lower than those necessary to reduce the sensory component. Although the neural mechanisms underlying the effects of morphine on the sensory component of pain have been investigated extensively, those influencing the affective component remain to be elucidated. The bed nucleus of the stria terminalis (BNST) has been implicated in the regulation of various negative emotional states, including aversion, anxiety and fear. Thus, this study aimed to clarify the role of the ventral part of the BNST (vBNST) in the actions of morphine on the affective and sensory components of pain. First, the effects of intra-vBNST injections of morphine on intraplantar formalin-induced conditioned place aversion (CPA) and nociceptive behaviors were investigated. Intra-vBNST injections of morphine reduced CPA without affecting nociceptive behaviors, which suggests that intra-vBNST morphine alters the affective, but not sensory, component of pain. Next, to examine the effects of morphine on neuronal excitability in type II vBNST neurons, whole-cell patch-clamp recordings were performed in brain slices. Bath application of morphine hyperpolarized type II vBNST neurons. Thus, the suppressive effects of intra-vBNST morphine on pain-induced aversion may be due to its inhibitory effects on neuronal excitability in type II vBNST neurons. These results suggest that the vBNST is a key brain region involved in the suppressive effects of morphine on the affective component of pain.

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“…We previously reported that CRF selectively depolarizes dlBNST type II neurons (Ide et al, 2013) and increases the inhibitory synaptic inputs to dlBNST type III neurons (Nagano et al, 2015) in naive rats. The present study showed that: (1) the sIPSC frequency in the VTA-projecting dlBNST type III neurons increased during chronic pain, (2) CRF increased the sIPSC frequency in the VTA-projecting dlBNST type III neurons of the shamoperated control, but not the chronic pain rats, suggesting the occlusion of the effect of exogenously applied CRF in the chronic pain group, and (3) NBI27914, a CRF type 1 receptor antagonist, decreased sIPSC frequency in the chronic pain, but not the control group.…”

Section: Discussionmentioning

confidence: 99%

Tonic Suppression of the Mesolimbic Dopaminergic System by Enhanced Corticotropin-Releasing Factor Signaling Within the Bed Nucleus of the Stria Terminalis in Chronic Pain Model Rats

et al. 2019

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Although dysfunction of the mesolimbic dopaminergic system has been implicated in chronic pain, the underlying mechanisms remain to be elucidated. We hypothesized that increased inhibitory inputs to the neuronal pathway from the dorsolateral bed nucleus of the stria terminalis (dlBNST) to the ventral tegmental area (VTA) during chronic pain may induce tonic suppression of the mesolimbic dopaminergic system. To test this hypothesis, male Sprague Dawley rats were subjected to spinal nerve ligation to induce neuropathic pain and then spontaneous IPSCs (sIPSCs) were measured in this neuronal pathway. Whole-cell patch-clamp electrophysiology of brain slices containing the dlBNST revealed that the frequency of sIPSCs significantly increased in VTA-projecting dlBNST neurons 4 weeks after surgery. Next, the role of corticotropin-releasing factor (CRF) signaling within the dlBNST in the increased sIPSCs was examined. CRF increased the frequency of sIPSCs in VTA-projecting dlBNST neurons in sham-operated controls, but not in chronic pain rats. By contrast, NBI27914, a CRF type 1 receptor antagonist, decreased the frequency of sIPSCs in VTA-projecting dlBNST neurons in the chronic pain rats, but not in the control animals. In addition, histological analyses revealed the increased expression of CRF mRNA in the dlBNST. Finally, bilateral injections of NBI27914 into the dlBNST of chronic pain rats activated mesolimbic dopaminergic neurons and induced conditioned place preference. Together, these results suggest that the mesolimbic dopaminergic system is tonically suppressed during chronic pain by enhanced CRF signaling within the dlBNST via increased inhibitory inputs to VTA-projecting dlBNST neurons.

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Corticotropin-releasing factor enhances inhibitory synaptic transmission to type III neurons in the bed nucleus of the stria terminalis

Cited by 15 publications

References 21 publications

Activation of the neural pathway from the dorsolateral bed nucleus of the stria terminalis to the central amygdala induces anxiety‐like behaviors

Activation of the neural pathway from the dorsolateral bed nucleus of the stria terminalis to the central amygdala induces anxiety‐like behaviors

Suppressive effects of morphine injected into the ventral bed nucleus of the stria terminalis on the affective, but not sensory, component of pain in rats

Tonic Suppression of the Mesolimbic Dopaminergic System by Enhanced Corticotropin-Releasing Factor Signaling Within the Bed Nucleus of the Stria Terminalis in Chronic Pain Model Rats

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