Phosphorylation-Dependent Low-Frequency Depression at Phasic Synapses of a Crayfish Motoneuron

Silverman‐Gavrila, Lorelei B.; Orth, Peter; Charlton, Milton P.

doi:10.1523/jneurosci.4908-04.2005

Cited by 19 publications

(39 citation statements)

References 60 publications

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“…In some crayfish neuromuscular synapses, a LFD occurred at 0.5 to 1 Hz, which was not likely related to depletion of synaptic vesicles (Bryan and Atwood 1981). In invertebrates, LFD has also been suggested to involve a shift in balance between phosphorylated and unphosphorylated substrates (Silverman-Gavrila and Charlton 2009;Silverman-Gavrila et al 2005). Our findings suggest that NMMII is a contributor to a form of LFD, which requires high-frequency conditioning.…”

Section: Discussionsupporting

confidence: 54%

Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction ofDrosophila

Seabrooke

Stewart

2011

Journal of Neurophysiology

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Seabrooke S, Stewart BA. Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction of Drosophila. J Neurophysiol 105: 1966 -1976, 2011. First published February 16, 2011 doi:10.1152/jn.00718.2010.-The synaptic vesicle population in a nerve terminal is traditionally divided into subpopulations according to physiological criteria; the readily releasable pool (RRP), the recycling pool, and the reserve pool. It is recognized that the RRP subserves synaptic transmission evoked by low-frequency neural activity and that the recycling and reserve populations are called on to supply vesicles as neural activity increases. Here we investigated the contribution of nonmuscle myosin II (NMMII) to synaptic transmission with emphasis on the role a motor protein could play in the supply of vesicles. We used Drosophila genetics to manipulate NMMII and assessed synaptic transmission at the larval neuromuscular junction. We observed a positive correlation between synaptic strength at low-frequency stimulation and NMMII expression: reducing NMMII reduced the evoked response, while increasing NMMII increased the evoked response. Further, we found that NMMII contributed to the spontaneous release of vesicles differentially from evoked release, suggesting differential contribution to these two release mechanisms. By measuring synaptic responses under conditions of differing external calcium concentration in saline, we found that NMMII is important for normal synaptic transmission under high-frequency stimulation. This research identifies diverse functions for NMMII in synaptic transmission and suggests that this motor protein is an active contributor to the physiology of synaptic vesicle recruitment.electrophysiology; low-frequency depression; high frequency; vesicle pools SYNAPTIC VESICLES ARE DESCRIBED as existing in three populations depending on how they participate is synaptic transmission (Rizzoli and Betz 2005). The readily releasable pool (RRP) of vesicles contains those vesicles that are released immediately upon action potential arrival at the nerve terminal. The RRP typically makes up 1-2% of the total vesicle pool and is rapidly depleted by repetitive stimulation. The recycling pool, com-

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Section: Discussionsupporting

confidence: 54%

Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction ofDrosophila

Seabrooke

Stewart

2011

Journal of Neurophysiology

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“…Comparison of LFD with other forms of homosynaptic depression The form of LFD described here is clearly reminiscent of the synaptic fatigue or LFD reported at other invertebrate and mammalian synapses (Silver et al, 1998;Saviane et al, 2002;Abrahamsson et al, 2005;Silverman-Gavrila et al, 2005;Silverman-Gavrila and Charlton, 2009). In all cases, LFD is induced at the same rate of stimulation (1 Hz) and stabilizes at a plateau-fixed level.…”

Section: Discussionsupporting

confidence: 52%

“…Interestingly, at mammalian synapses, the all-or-none feature of presynaptic adaptation has been proposed to result from changes in SV priming (Moulder et al, 2006). Moreover, at phasic synapses of a crayfish motoneuron, LFD is induced by an activity-dependent dephosphorylation of proteins involved in neurotransmitter release (Silverman-Gavrila et al, 2005). Therefore, a progressive and activity-dependent dephosphorylation of proteins involved in priming may lead to a silencing of presynaptic release sites.…”

Section: Mechanisms Underlying the Switching Off Of Release Sitesmentioning

confidence: 99%

A Novel Form of Presynaptic Plasticity Based on the Fast Reactivation of Release Sites Switched Off during Low-Frequency Depression

Doussau

Humeau²,

Benfenati³

et al. 2010

J. Neurosci.

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Repetitive firing of neurons at a low frequency often leads to a decrease in synaptic strength. The mechanism of this low-frequency depression (LFD) is poorly understood. Here, LFD was studied at Aplysia cholinergic synapses. The absence of a significant change in the paired-pulse ratio during LFD, together with the facts that neither the time course nor the extent of LFD were affected by the initial release probability, suggests that LFD is not related to a depletion of the ready-to-fuse synaptic vesicles (SVs) or to a decrease in the release probability, but results from the silencing of a subpopulation of release sites. A subset of SVs or release sites, which acquired a high release probability status during LFD, permits synapses to rapidly and temporarily recover the initial synaptic strength when the stimulation is stopped. However, the recovery of the full capacity of the synapse to sustain repetitive stimulations is slow and involves spontaneous reactivation of the silent release sites. Application of tetanic stimulations accelerates this recovery by immediately switching on the silent sites. This high-frequency-dependent phenomenon underlies a new form of synaptic plasticity that allows resetting of presynaptic efficiency independently of the recent history of the synapse. Microinjection of a mutated Aplysia synapsin that cannot be phosphorylated by cAMP-dependent protein kinase (PKA), or a PKA inhibitor both prevented high-frequency-dependent awakening of release sites. Changes in the firing pattern of neurons appear to be able to regulate the on-off status of release sites via a molecular cascade involving PKA-dependent phosphorylation of synapsin.

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“…Bauman et al, 2000;Munton et al, 2004). Protein phosphatases may also act presynaptically to regulate neurotransmitter release (Sistiaga and Sanchez-Prieto, 2000;Silverman-Gavrila et al, 2005). The techniques used in this study do not allow us to address the specific actions of the relevant serine/threonine protein phosphatases.…”

Section: Working Model Of Phrenic Ltf and Pattern Sensitivitymentioning

confidence: 99%

Okadaic Acid-Sensitive Protein Phosphatases Constrain Phrenic Long-Term Facilitation after Sustained Hypoxia

Wilkerson¹,

Satriotomo²,

Baker-Herman³

et al. 2008

J. Neurosci.

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Phrenic long-term facilitation (pLTF) is a serotonin-dependent form of pattern-sensitive respiratory plasticity induced by intermittent hypoxia (IH), but not sustained hypoxia (SH). The mechanism(s) underlying pLTF pattern sensitivity are unknown. SH and IH may differentially regulate serine/threonine protein phosphatase activity, thereby inhibiting relevant protein phosphatases uniquely during IH and conferring pattern sensitivity to pLTF. We hypothesized that spinal protein phosphatase inhibition would relieve this braking action of protein phosphatases, thereby revealing pLTF after SH. Anesthetized rats received intrathecal (C4) okadaic acid (25 nM) before SH (25 min, 11% O 2 ). Unlike (vehicle) control rats, SH induced a significant pLTF in okadaic acid-treated rats that was indistinguishable from rats exposed to IH (three 5 min episodes, 11% O 2 ). IH and SH with okadaic acid may elicit pLTF by similar, serotonin-dependent mechanisms, because intravenous methysergide blocks pLTF in rats receiving IH or okadaic acid plus SH. Okadaic acid did not alter IH-induced pLTF. In summary, pattern sensitivity in pLTF may reflect differential regulation of okadaic acid-sensitive serine/threonine phosphatases; presumably, these phosphatases are less active during/after IH versus SH. The specific okadaic acid-sensitive phosphatase(s) constraining pLTF and their spatiotemporal dynamics during and/or after IH and SH remain to be determined.

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Phosphorylation-Dependent Low-Frequency Depression at Phasic Synapses of a Crayfish Motoneuron

Cited by 19 publications

References 60 publications

Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction ofDrosophila

Synaptic transmission and plasticity are modulated by nonmuscle myosin II at the neuromuscular junction ofDrosophila

A Novel Form of Presynaptic Plasticity Based on the Fast Reactivation of Release Sites Switched Off during Low-Frequency Depression

Okadaic Acid-Sensitive Protein Phosphatases Constrain Phrenic Long-Term Facilitation after Sustained Hypoxia

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