Repolarization of the presynaptic action potential and short‐term synaptic plasticity in the chick ciliary ganglion

Poage, Robert E.; Zengel, J E

doi:10.1002/syn.10135

Cited by 4 publications

(7 citation statements)

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“…We tested this idea using extracellular recordings (Figure S7) of compound APs (cAPs, also known as fiber volleys) and resulting field EPSPs (fEPSPs) in the CA1 stratum radiatum, the location of CA3 PC axons and synaptic terminals. The cAP is essentially proportional to the time derivative of membrane voltage during AP firing and the cAP amplitude can be used as a surrogate for AP duration (Bean, 2007; Poage and Zengel, 2002). We found that cAP amplitude was excessively increased during high-frequency trains in the Fmr1 KO relative to WT mice (Figures 8A,B, Table S1; n=10(WT),11(KO); p=0.0015), in close agreement with our somatic AP recordings (Figure 1B).…”

Section: Resultsmentioning

confidence: 99%

FMRP Regulates Neurotransmitter Release and Synaptic Information Transmission by Modulating Action Potential Duration via BK Channels

Deng

Rotman

Blundon

et al. 2013

Neuron

316

324

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SUMMARY Loss of FMRP causes Fragile X syndrome (FXS), but the physiological functions of FMRP remain highly debatable. Here we show that FMRP regulates neurotransmitter release in CA3 pyramidal neurons by modulating action potential (AP) duration. Loss of FMRP leads to excessive AP broadening during repetitive activity, enhanced presynaptic calcium influx and elevated neurotransmitter release. The AP broadening defects caused by FMRP loss have a cell-autonomous presynaptic origin and can be acutely rescued in postnatal neurons. These presynaptic actions of FMRP are translation-independent and are mediated selectively by BK channels via interaction of FMRP with BK channel’s regulatory β4 subunits. Information-theoretical analysis demonstrates that loss of these FMRP functions causes marked dysregulation of synaptic information transmission. FMRP-dependent AP broadening is not limited to the hippocampus, but also occurs in cortical pyramidal neurons. Our results thus suggest major translation-independent presynaptic functions of FMRP that may have important implications for understanding FXS neuropathology.

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Section: Resultsmentioning

confidence: 99%

FMRP Regulates Neurotransmitter Release and Synaptic Information Transmission by Modulating Action Potential Duration via BK Channels

Deng

Rotman

Blundon

et al. 2013

Neuron

316

324

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“…The initially reduced excitability may be due to an AHP. Both peripheral unmyelinated axons (Frankenheuser & Hodgkin, 1956; Greengard & Straub, 1958) and some pre‐synaptic terminals (Forsythe, 1994; Poage & Zengel, 2002) show AHPs after single action potentials.…”

Section: Discussionmentioning

confidence: 99%

“…Furthermore, such pre‐synaptic after‐potentials can influence transmitter release. This has been demonstrated in the chick ciliary ganglion (Poage & Zengel, 2002) and at the crayfish neuromuscular junction (Wojtowicz & Atwood, 1983, 1984; Blundon et al 1995; Vyshedskiy & Lin, 1997) where small hyperpolarizing or depolarizing pulses applied before the action potential influenced transmitter release.…”

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confidence: 87%

“…Recordings from large pre‐synaptic terminals in invertebrates and mammalian CNS have demonstrated that AHPs and ADPs can follow the action potentials (Marsal et al 1997; Wojtowicz & Atwood, 1983, 1984; Forsythe, 1994; Borst & Sakmann, 1996, 1998; Geiger & Jonas, 2000; Poage & Zengel, 2002). Furthermore, such pre‐synaptic after‐potentials can influence transmitter release.…”

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confidence: 99%

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Activity‐dependent excitability changes in hippocampal CA3 cell Schaffer axons

Soleng

Baginskas

Andersen

et al. 2004

The Journal of Physiology

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The membrane potential changes following action potentials in thin unmyelinated cortical axons with en passant boutons may be important for synaptic release and conduction abilities of such axons. In the lack of intra-axonal recording techniques we have used extracellular excitability testing as an indirect measure of the after-potentials. We recorded from individual CA3 soma in hippocampal slices and activated the axon with a range of stimulus intensities. When conditioning and test stimuli were given to the same site the excitability changes were partly masked by local effects of the stimulating electrode at intervals < 5 ms. Therefore, we elicited the conditioning action potential from one axonal branch and tested the excitability of another branch. We found that a single action potential reduced the axonal excitability for 15 ms followed by an increased excitability for ∼200 ms at 24• C. Using field recordings of axonal action potentials we show that raising the temperature to 34• C reduced the magnitude and duration of the initial depression. However, the duration of the increased excitability was very similar (time constant 135 ± 20 ms) at 24 and 34• C, and with 2.0 and 0.5 mM Ca 2+ in the bath. At stimulus rates > 1 Hz, a condition that activates a hyperpolarization-activated current (I h ) in these axons, the decay was faster than at lower stimulation rates. This effect was reduced by the I h blocker ZD7288. These data suggest that the decay time course of the action potential-induced hyperexcitability is determined by the membrane time constant.

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“…Following the AP, the membrane potential during the recovery period has a large influence on the speed of the recovery from inactivation of voltage-dependent sodium channels and deactivation of voltagedependent potassium channels, which are two major determinants of the refractory period (2). In some terminals, the AP is followed by a depolarizing afterpotential (DAP) (3)(4)(5)(6)(7)(8)(9), whereas in others a hyperpolarizing afterpotential (HAP) has been observed (10)(11)(12)(13)(14). The sign of this afterpotential depends on the resting potential (6,7,15), suggesting that the membrane potential following the AP (V after ) might be more important than the sign of the afterpotential.…”

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confidence: 99%

Resistance to action potential depression of a rat axon terminal in vivo

Sierksma

Borst

2017

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

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The shape of the presynaptic action potential (AP) has a strong impact on neurotransmitter release. Because of the small size of most terminals in the central nervous system, little is known about the regulation of their AP shape during natural firing patterns in vivo. The calyx of Held is a giant axosomatic terminal in the auditory brainstem, whose biophysical properties have been well studied in slices. Here, we made whole-cell recordings from calyceal terminals in newborn rat pups. The calyx showed a characteristic burst firing pattern, which has previously been shown to originate from the cochlea. Surprisingly, even for frequencies over 200 Hz, the AP showed little or no depression. Current injections showed that the rate of rise of the AP depended strongly on its onset potential, and that the membrane potential after the AP (V after ) was close to the value at which no depression would occur during high-frequency activity. Immunolabeling revealed that Na v 1.6 is already present at the calyx shortly after its formation, which was in line with the fast recovery from AP depression that we observed in slice recordings. Our findings thus indicate that fast recovery from depression and an inter-AP membrane potential that minimizes changes on the next AP in vivo, together enable high timing precision of the calyx of Held already shortly after its formation.A ction potentials (APs) are followed by a period of decreased excitability called the refractory period. High-frequency firing thus requires special adaptations to minimize this refractory period and maintain AP stability. The changes in the AP waveform that occur at high firing frequencies are especially relevant in presynaptic terminals, where the shape of the AP critically controls calcium influx via voltage-dependent calcium channels, and thus transmitter release (1, 2). Following the AP, the membrane potential during the recovery period has a large influence on the speed of the recovery from inactivation of voltage-dependent sodium channels and deactivation of voltagedependent potassium channels, which are two major determinants of the refractory period (2). In some terminals, the AP is followed by a depolarizing afterpotential (DAP) (3-9), whereas in others a hyperpolarizing afterpotential (HAP) has been observed (10-14). The sign of this afterpotential depends on the resting potential (6,7,15), suggesting that the membrane potential following the AP (V after ) might be more important than the sign of the afterpotential.The calyx of Held is a glutamatergic axosomatic terminal whose biophysical properties have been well studied (16). Its many release sites enable it to act as an inverting relay synapse within the auditory brainstem that reliably drives its postsynaptic partner, a principal neuron in the medial nucleus of the trapezoid body (MNTB), even at firing frequencies >200 Hz (17). Shortly after its formation, around postnatal day 2 (P2) in rodents (18)(19)(20), it already fires in characteristic high-frequency bursts in vivo (21,22). In slice studi...

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Repolarization of the presynaptic action potential and short‐term synaptic plasticity in the chick ciliary ganglion

Cited by 4 publications

References 94 publications

FMRP Regulates Neurotransmitter Release and Synaptic Information Transmission by Modulating Action Potential Duration via BK Channels

FMRP Regulates Neurotransmitter Release and Synaptic Information Transmission by Modulating Action Potential Duration via BK Channels

Activity‐dependent excitability changes in hippocampal CA3 cell Schaffer axons

Resistance to action potential depression of a rat axon terminal in vivo

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