Glutamatergic Modulation of Cerebellar Interneuron Activity Is Mediated by an Enhancement of GABA Release and Requires Protein Kinase A/RIM1α Signaling

Lachamp, Philippe; Liu, Yu; Liu, Siqiong June

doi:10.1523/jneurosci.2354-08.2009

Cited by 43 publications

(52 citation statements)

References 67 publications

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“…Food deprivation also led to a significant increase in the coefficient of variation (CV −2 ) of synaptic current amplitude (Fig. 2D), consistent with a presynaptic modulation of transmitter release probability (16,17).…”

Section: Significancesupporting

confidence: 63%

Fasting induces a form of autonomic synaptic plasticity that prevents hypoglycemia

Wang

Whim

2016

Proc. Natl. Acad. Sci. U.S.A.

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During fasting, activation of the counter-regulatory response (CRR) prevents hypoglycemia. A major effector arm is the autonomic nervous system that controls epinephrine release from adrenal chromaffin cells and, consequently, hepatic glucose production. However, whether modulation of autonomic function determines the relative strength of the CRR, and thus the ability to withstand food deprivation and maintain euglycemia, is not known. Here we show that fasting leads to altered transmission at the preganglionic → chromaffin cell synapse. The dominant effect is a presynaptic, long-lasting increase in synaptic strength. Using genetic and pharmacological approaches we show this plasticity requires neuropeptide Y, an adrenal cotransmitter and the activation of adrenal Y5 receptors. Loss of neuropeptide Y prevents a fasting-induced increase in epinephrine release and results in hypoglycemia in vivo. These findings connect plasticity within the sympathetic nervous system to a physiological output and indicate the strength of the final synapse in this descending pathway plays a decisive role in maintaining euglycemia.hypoglycemia | autonomic nervous system | synaptic plasticity | adrenal | chromaffin cells F ailure to avoid hypoglycemia can lead to dysphoria, ventricular arrhythmia, and even sudden death (1). That these effects are rare and observed only in response to prolonged fasting or severe insulin-induced hypoglycemia is because of the remarkable effectiveness of the counter-regulatory response (CRR). This sensory-motor homeostatic feedback loop detects a fall in blood glucose through central and peripheral receptors and initiates a neuronal, endocrine, and behavioral response that restores euglycemia (2). One of the principal effector arms of the CRR is the sympatho-adrenal branch of the autonomic nervous system. Hypoglycemia elevates sympathetic activity, increasing hepatic glucose production and the release of gluconeogenic substrates while suppressing insulin and potentiating glucagon secretion (3, 4).During fasting, these autonomic actions are mediated by epinephrine, which enters the systemic circulation after release from adrenal neuroendocrine chromaffin cells and by norepinephrine, secreted directly onto target tissues from postganglionic sympathetic neurons. The importance of sympathetic activity, and in particular circulating epinephrine in the CRR, is illustrated by the poor recovery from insulin-induced hypoglycemia when the release of this hormone is suppressed during hypoglycemia-associated autonomic failure (5, 6), and by recent work showing that deletion of melanocortin 4 receptors from preganglionic sympathetic neurons leads to elevated levels of blood glucose (7).Given the involvement of the sympathetic nervous system in the CRR, modulation of autonomic activity is thus likely to alter the ability to respond to a hypoglycemic challenge. However, unlike in the CNS, where long-lasting changes in synaptic strength are known to be associated with functional consequences (8-10), whether the output ...

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Section: Significancesupporting

confidence: 63%

Fasting induces a form of autonomic synaptic plasticity that prevents hypoglycemia

Wang

Whim

2016

Proc. Natl. Acad. Sci. U.S.A.

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“…In rodent cerebellar cortex, glutamate released from parallel fibers induces a long-lasting increase of GABA release from stellate cells, presumably by activating preNMDARs on their terminals (Liu and Lachamp 2006). This heterosynaptic form of LTP also requires cAMP/PKA signaling (Lachamp et al 2009). Finally, in the developing Xenopus retinotectal system, light stimuli or theta burst stimulation of the optic nerve triggers presynaptic LTD of GABAergic synaptic transmission on tectal neurons (Lien et al 2006).…”

Section: Presynaptic Nmdar-dependent Plasticitymentioning

confidence: 99%

“…As a result, RIM1a is in a strategic position to modulate transmitter release (Koushika et al 2001;Schoch et al 2002). Indeed, RIM1a has been shown to be necessary for several cAMP/PKA-dependent forms of presynaptic plasticity including, MF-LTP , cerebellar PF-LTP , MF-SLIN LTP or de-depression (Pelkey et al 2008), associative LTP in lateral amygdala (Fourcaudot et al 2008), late LTP at Sch-CA1 synapses (Huang et al 2005), GABAergic LTP at stellate cells in cerebellum (Lachamp et al 2009), and inhibitory eCB-LTD in the hippocampus and amygdala (Chevaleyre et al 2007). In addition, RIM1a is a putative effector for the synaptic vesicle protein Rab3A, a protein essential for MF-LTP (Castillo et al 1997), MF-LTD (Tzounopoulos et al 1998), and late-LTP in CA1 (Huang et al 2005).…”

Section: Changes In the Release Machinerymentioning

confidence: 99%

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Castillo

2011

Cold Spring Harbor Perspectives in Biology

132

134

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Ubiquitous forms of long-term potentiation (LTP) and depression (LTD) are caused by enduring increases or decreases in neurotransmitter release. Such forms or presynaptic plasticity are equally observed at excitatory and inhibitory synapses and the list of locations expressing presynaptic LTP and LTD continues to grow. In addition to the mechanistically distinct forms of postsynaptic plasticity, presynaptic plasticity offers a powerful means to modify neural circuits. A wide range of induction mechanisms has been identified, some of which occur entirely in the presynaptic terminal, whereas others require retrograde signaling from the postsynaptic to presynaptic terminals. In spite of this diversity of induction mechanisms, some common induction rules can be identified across synapses. Although the precise molecular mechanism underlying long-term changes in transmitter release in most cases remains unclear, increasing evidence indicates that presynaptic LTP and LTD can occur in vivo and likely mediate some forms of learning.A t several excitatory and inhibitory synapses, neuronal activity can trigger enduring increases or decreases in neurotransmitter release, thereby producing long-term potentiation (LTP) or long-term depression (LTD) of synaptic strength, respectively. In the last decade, many studies have revealed that these forms of plasticity are ubiquitously expressed in the mammalian brain, and accumulating evidence indicates that they may underlie behavioral adaptations occurring in vivo. These studies have also uncovered a wide range of induction mechanisms, which converge on the presynaptic terminal where an enduring modification in the neurotransmitter release process takes place. Interestingly, presynaptic forms of LTP/ LTD can coexist with classical forms of postsynaptic plasticity. Such diversity expands the dynamic range and repertoire by which neurons modify their synaptic connections. This review discusses mechanistic aspects of presynaptic LTP and LTD at both excitatory and inhibitory synapses in the mammalian brain, with an emphasis on recent findings. INDUCTION MECHANISMSAs illustrated in Figure 1, presynaptic LTP/LTD at both excitatory and inhibitory synapses can be induced in a homosynaptic or heterosynaptic manner, with induction occurring either entirely at the presynaptic terminal or requiring a retrograde messenger arising from the postsynaptic neuron. Each of these four induction

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“…In excitatory CA3-region mossy fiber synapses, cerebellar parallel fiber synapses, and cortico-lateral amygdala synapses, RIM1 is necessary for presynaptic long term plasticity. Using pharmacological and genetic approaches, a presynaptic signaling pathway via cAMP, protein kinase A, and RIM1␣ was elucidated as a general mechanism that underlies the long term modulation of transmitter release at both excitatory and inhibitory synapses (46). In autapses, the RIM1␣ deletion significantly reduces the readily releasable pool of vesicles, and it alters short term plasticity and the properties of evoked asynchronous release (47).…”

Section: Assembly Of Voltage-dependent Camentioning

confidence: 99%

Rab3-interacting Molecule γ Isoforms Lacking the Rab3-binding Domain Induce Long Lasting Currents but Block Neurotransmitter Vesicle Anchoring in Voltage-dependent P/Q-type Ca2+ Channels

Uriu

Kiyonaka

Miki

et al. 2010

Journal of Biological Chemistry

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Glutamatergic Modulation of Cerebellar Interneuron Activity Is Mediated by an Enhancement of GABA Release and Requires Protein Kinase A/RIM1α Signaling

Cited by 43 publications

References 67 publications

Fasting induces a form of autonomic synaptic plasticity that prevents hypoglycemia

Fasting induces a form of autonomic synaptic plasticity that prevents hypoglycemia

Presynaptic LTP and LTD of Excitatory and Inhibitory Synapses

Rab3-interacting Molecule γ Isoforms Lacking the Rab3-binding Domain Induce Long Lasting Currents but Block Neurotransmitter Vesicle Anchoring in Voltage-dependent P/Q-type Ca2+ Channels

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