Modulation of SK Channel Trafficking by Beta Adrenoceptors Enhances Excitatory Synaptic Transmission and Plasticity in the Amygdala

Faber, E. S. L.; Delaney, Andrew; Power, John M.; Sedlak, Petra L.; Crane, James W.; Sah, Pankaj

doi:10.1523/jneurosci.1796-08.2008

Cited by 101 publications

(102 citation statements)

References 67 publications

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“…Because activation of SK channels by ACh negatively regulates cell excitability (Nenov et al, 1996;Nakajima et al, 2007), it is tempting to speculate that SK channels shorten the depolarizing action of synaptically released ACh, thereby preventing the formation of a depolarizing plateau in case of high-frequency synaptic activity at the splanchnic nerve-chromaffin cell junction. On the other hand, one could propose that ␣9-containing nAChRs modulate SK channel trafficking and remove them from synapses, as described for ␤-adrenoceptors (Faber et al, 2008). Thus, cholinergic neurotransmission at the splanchnic synapses would initially be more robust.…”

Section: Discussionmentioning

confidence: 99%

Functional Characterization of α9-Containing Cholinergic Nicotinic Receptors in the Rat Adrenal Medulla: Implication in Stress-Induced Functional Plasticity

Colomer

Olivos-Oré²,

Vincent³

et al. 2010

J. Neurosci.

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An increase in circulating adrenal catecholamine levels constitutes one of the mechanisms whereby organisms cope with stress. Accordingly, stimulus-secretion coupling within the stressed adrenal medullary tissue undergoes persistent remodeling. In particular, cholinergic synaptic neurotransmission between splanchnic nerve terminals and chromaffin cells is upregulated in stressed rats. Since synaptic transmission is mainly supported by activation of postsynaptic neuronal acetylcholine nicotinic receptors (nAChRs), we focused our study on the role of ␣9-containing nAChRs, which have been recently described in chromaffin cells. Taking advantage of their specific blockade by the ␣-conotoxin RgIA (␣-RgIA), we unveil novel functional roles for these receptors in the stimulus-secretion coupling of the medulla. First, we show that in rat acute adrenal slices, ␣9-containing nAChRs codistribute with synaptophysin and significantly contribute to EPSCs. Second, we show that these receptors are involved in the tonic inhibitory control exerted by cholinergic activity on gap junctional coupling between chromaffin cells, as evidenced by an increased Lucifer yellow diffusion within the medulla in ␣-RgIA-treated slices. Third, we unexpectedly found that ␣9-containing nAChRs dominantly (Ͼ70%) contribute to acetylcholine-induced current in cold-stressed rats, whereas ␣3 nAChRs are the main contributing channels in unstressed animals. Consistently, expression levels of ␣9 nAChR transcript and protein are overexpressed in cold-stressed rats. As a functional relevance, we propose that upregulation of ␣9-containing nAChR channels and ensuing dominant contribution in cholinergic signaling may be one of the mechanisms whereby adrenal medullary tissue appropriately adapts to increased splanchnic nerve electrical discharges occurring in stressful situations.

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Section: Discussionmentioning

confidence: 99%

Functional Characterization of α9-Containing Cholinergic Nicotinic Receptors in the Rat Adrenal Medulla: Implication in Stress-Induced Functional Plasticity

Colomer

Olivos-Oré²,

Vincent³

et al. 2010

J. Neurosci.

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“…Activation of badrenergic receptors (Faber et al, 2008), activation of PKA (Ren et al, 2006), and neuronal activity (Lin et al, 2010) all modify the expression of SK channel subunits. Perhaps, the differences in the effects of repeated stress on these factors in adult and adolescent neurons between the BA and LA contribute to these age-and nucleus-specific differences.…”

Section: Discussionmentioning

confidence: 99%

Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

Hetzel

Rosenkranz

2014

Neuropsychopharmacol

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Severe and repeated stress has damaging effects on health, including initiation of depression and anxiety. Stress that occurs during development has long-lasting and particularly damaging effects on emotion. The basolateral amygdala (BLA) plays a key role in many affective behaviors, and repeated stress causes different forms of BLA hyperactivity in adolescent and adult rats. However, the mechanism is not known. Furthermore, not every individual is susceptible to the negative consequences of stress. Differences in the effects of stress on the BLA might contribute to determine whether an individual will be vulnerable or resilient to the effects of stress on emotion. The purpose of this study is to test the cellular underpinnings for age dependency of BLA hyperactivity after stress, and whether protective changes occur in resilient individuals. To test this, the effects of repeated stress on membrane excitability and other membrane properties of BLA principal neurons were compared between adult and adolescent rats, and between vulnerable and resilient rats, using in vitro whole-cell recordings. Vulnerability was defined by adrenal gland weight, and verified by body weight gain after repeated restraint stress, and fecal pellet production during repeated restraint sessions. We found that repeated stress increased the excitability of BLA neurons, but in a manner that depended on age and BLA subnucleus. Furthermore, stress resilience was associated with an opposite pattern of change, with increased slow afterhyperpolarization (AHP) potential, whereas vulnerability was associated with decreased medium AHP. The opposite outcomes in these two populations were further distinguished by differences of anxiety-like behavior in the elevated plus maze that were correlated with BLA neuronal excitability and AHP. These results demonstrate a substrate for BLA hyperactivity after repeated stress, with distinct membrane properties to target, as well as age-dependent factors that contribute to resilience to the effects of stress.

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“…In addition, the back-propagation of somatically generated action potentials into pyramidal cell dendrites is another potentially important source of postsynaptic depolarization needed for NMDAR activation and LTP induction (Watanabe et al 2002) and dendritically localized Kv4.2/A-type potassium channels can strongly attenuate action potential back-propagation (Hoffman et al 1997;Chen et al 2006). b-AR activation inhibits both SK2 and Kv4.2 potassium channels through effects mediated by PKA and ERK (Hoffman and Johnston 1999;Yuan et al 2002;Faber et al 2008), thus providing a mechanism whereby b-AR activation can boost spine depolarization at active synapses and facilitate LTP induction by enhancing NMDAR activation.…”

Section: Molecular Mechanisms Underlying the Enhancement Of Ltp By B-mentioning

confidence: 99%

β-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus

et al. 2015

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Encoding new information in the brain requires changes in synaptic strength. Neuromodulatory transmitters can facilitate synaptic plasticity by modifying the actions and expression of specific signaling cascades, transmitter receptors and their associated signaling complexes, genes, and effector proteins. One critical neuromodulator in the mammalian brain is norepinephrine (NE), which regulates multiple brain functions such as attention, perception, arousal, sleep, learning, and memory. The mammalian hippocampus receives noradrenergic innervation and hippocampal neurons express b-adrenergic receptors, which are known to play important roles in gating the induction of long-lasting forms of synaptic potentiation. These forms of long-term potentiation (LTP) are believed to importantly contribute to long-term storage of spatial and contextual memories in the brain. In this review, we highlight the contributions of noradrenergic signaling in general and b-adrenergic receptors in particular, toward modulating hippocampal LTP. We focus on the roles of NE and b-adrenergic receptors in altering the efficacies of specific signaling molecules such as NMDA and AMPA receptors, protein phosphatases, and translation initiation factors. Also, the roles of b-adrenergic receptors in regulating synaptic "tagging" and "capture" of LTP within synaptic networks of the hippocampus are reviewed. Understanding the molecular and cellular bases of noradrenergic signaling will enrich our grasp of how the brain makes new, enduring memories, and may shed light on credible strategies for improving mental health through treatment of specific disorders linked to perturbed memory processing and dysfunctional noradrenergic synaptic transmission.Synaptic plasticity is a fundamental property of nervous system function. A neuron's ability to alter the strength of its synaptic connections is thought to be the foundation for multiple processes, including learning and memory. Synaptic plasticity is not a single, unitary cellular process, but rather an extremely diverse phenomenon that encompasses many forms and functions. Synapses are dynamic by nature, and only through elucidation of the mechanisms that govern their organization and reorganization can we hope to fully understand how the brain processes and stores information.Acting as potent regulatory agents, neuromodulatory transmitters can significantly alter the properties of neurons at cellular and network levels. Specifically, the modulatory role of the noradrenergic system has been extensively characterized, in part because of the system's anatomically ubiquitous connections. Noradrenergic fibers originate mainly in the locus coeruleus (LC) and project widely throughout the forebrain, with dense innervation of the hippocampus, amygdala, and thalamus (Sara 2009). These connections, especially within the hippocampus, strongly modulate synaptic strength and neural network physiology, which lead to significant alterations in learning, memory, attention, and perception. Noradrenergic receptor signal...

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Modulation of SK Channel Trafficking by Beta Adrenoceptors Enhances Excitatory Synaptic Transmission and Plasticity in the Amygdala

Cited by 101 publications

References 67 publications

Functional Characterization of α9-Containing Cholinergic Nicotinic Receptors in the Rat Adrenal Medulla: Implication in Stress-Induced Functional Plasticity

Functional Characterization of α9-Containing Cholinergic Nicotinic Receptors in the Rat Adrenal Medulla: Implication in Stress-Induced Functional Plasticity

Distinct Effects of Repeated Restraint Stress on Basolateral Amygdala Neuronal Membrane Properties in Resilient Adolescent and Adult Rats

β-Adrenergic receptor signaling and modulation of long-term potentiation in the mammalian hippocampus

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