Developmental Changes in Short-Term Plasticity at the Rat Calyx of Held Synapse

Crins, T. T. H.; Rusu, Silviu I.; Rodríguez-Contreras, Adrián; Borst, Jannie

doi:10.1523/jneurosci.1995-11.2011

Cited by 50 publications

(74 citation statements)

References 80 publications

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“…Interestingly, the time course of changes in density of EdU-labeled cells described in this study (Fig. 4B) is similar to the time course of changes in spontaneous patterned activity described in the rodent auditory system (Sonntag et al, 2009;Crins et al, 2011). Studies are under way in our laboratory to determine the origin of small GFAP-labeled particles in the MNTB and their relationship to activity-dependent synaptic maturation.…”

Section: Progenitors In Mammalian Auditory Brainstemsupporting

confidence: 82%

“…To test the hypothesis that changes in auditory brainstem cell proliferation are linked to hearing development, we compared the pattern of postnatal cell proliferation in the rat MNTB with mice, gerbils, and ferrets. In these species, opening of the ear canal and hearing onset occur postnatally at different ages (postnatal day [P]13 for Wistar rats, Crins et al, 2011; our unpublished results; P12 for CBA/CaJ mice, Sonntag et al, 2009; P12 for gerbils, Woolf and Ryan, 1984;McGuirt et al, 1995;McFadden et al, 1996; P28 for ferrets, Moore and Hine, 1992). We performed further lesion experiments in rats with the goal to disrupt activity related signals in the auditory system and to examine their effects on cell proliferation in the MNTB.…”

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confidence: 99%

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Natural and lesion‐induced decrease in cell proliferation in the medial nucleus of the trapezoid body during hearing development

Saliu

Adise

Xian

et al. 2014

J of Comparative Neurology

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The functional interactions between neurons and glial cells that are important for nervous system function are presumably established during development from the activity of progenitor cells. In this study we examined proliferation of progenitor cells in the medial nucleus of the trapezoid body (MNTB) located in the rat auditory brainstem. We performed DNA synthesis labeling experiments to demonstrate changes in cell proliferation activity during postnatal stages of development. An increase in cell proliferation correlated with MNTB growth and the presence of S100b-positive astrocytes among MNTB neurons. In additional experiments we analyzed the fate of newly born cells. At perinatal ages, newly born cells colabeled with the astrocyte marker S100b in higher numbers than when cells were generated at postnatal day 6. Furthermore, we identified newly born cells that were colabeled with caspase-3 immunohistochemistry and performed comparative experiments to demonstrate that there is a natural decrease in cell proliferation activity during postnatal development in rats, mice, gerbils, and ferrets. Lastly, we found that there is a stronger decrease in MNTB cell proliferation after performing bilateral lesions of the auditory periphery in rats. Altogether, these results identify important stages in the development of astrocytes in the MNTB and provide evidence that the proliferative activity of the progenitor cells is developmentally regulated. We propose that the developmental reduction in cell proliferation may reflect coordinated signaling between the auditory brainstem and the auditory periphery. J. Comp. Neurol. 522:971-985, 2014.

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Section: Progenitors In Mammalian Auditory Brainstemsupporting

confidence: 82%

mentioning

confidence: 99%

Natural and lesion‐induced decrease in cell proliferation in the medial nucleus of the trapezoid body during hearing development

Saliu

Adise

Xian

et al. 2014

J of Comparative Neurology

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“…The reduced contribution of CDR at the mature calyx is in line with previous findings regarding a developmental decrease in the Ca 2+ -dependent modulation of presynaptic Ca 2+ channels (19,37) and short-term plasticity (38,39). Given that full depletion of the SRP is unlikely under physiological conditions in vivo (38), the SRP may play an important role in supplying SVs to the FRP and thus may be responsible for the reduced short-term depression observed in the mature calyx of Held synapse (38). Therefore, SDR may be essential for maintaining the background EPSC amplitude under in vivo conditions, when the calyx is invaded constantly by low-frequency APs.…”

supporting

confidence: 91%

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

Lee

2012

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

105

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Glutamatergic synaptic terminals harbor reluctant synaptic vesicles (SVs) that contribute little to synchronous release during action potentials but are release competent when stimulated by sucrose or by direct intracellular application of calcium. It has been noted that the proximity of a release-competent SV to the calcium source is one of the primary factors that differentiate reluctant SVs from fastreleasing ones at the calyx of Held synapse. It has not been known whether reluctant SVs can be converted into fast-releasing ones. Here we show that reluctant SVs are recruited rapidly in an actindependent manner to become fast-releasing SVs once the pool of fast-releasing SVs is depleted by a short depolarization. Recovery of the pool of fast-releasing SVs was accompanied by a parallel reduction in the number of reluctant SVs. Quantitative analysis of the time course of depletion of fast-releasing SVs during high-frequency stimulation revealed that in the early phase of stimulation reluctant SVs are converted rapidly into fast-releasing ones, thereby counteracting short-term depression. During the late phase, however, after reluctant vesicles have been used up, another process of calmodulindependent recruitment of fast-releasing SVs is activated. These results document that reluctant SVs have a role in short-term plasticity and support the hypothesis of positional priming, which posits that reluctant vesicles are converted into fast-releasing ones via relocation closer to Ca 2+ -channels.readily releasable pool | synaptic vesicle dynamics S ynaptic strength is determined by quantal size, the number of release-competent synaptic vesicles (SVs), and their release probability (Pr). The estimate for the number of release-competent SVs, which also is referred to as the "readily releasable pool (RRP) size," depends heavily on the method used for its determination. The RRP size estimated by a cumulative plot of the excitatory postsynaptic currents (EPSC) amplitudes evoked by high-frequency afferent fiber stimulation (RRP cum ) is smaller than that estimated by the application of a hypertonic sucrose solution or presynaptic strong depolarization (1-3). This discrepancy reflects the presence of reluctant SVs, which are scarcely released by an action potential (AP) at glutamatergic synaptic terminals. Consistently, deconvolution analysis of EPSCs evoked by a long depolarizing pulse at the calyx of Held revealed that release-competent SVs can be separated into fast-and slowreleasing SV pools (FRP and SRP, respectively) (4). The FRP vesicles are responsible for phasic release during a high-frequency train of action potentials (APs), whereas the SRP vesicles contribute primarily to asynchronous release, when the intracellular concentration of calcium ions ([Ca 2+ ]) is increased globally during the late period of the train (2). Thus, SRP vesicles can be regarded largely as reluctant SVs at the calyx of Held.Despite the evidence for the presence of reluctant SVs at glutamatergic synapses, their role in short-term plasticity i...

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“…Fourth, the terminals showed a characteristic firing pattern, consisting of minibursts with high firing frequencies ( Fig. 1D) (22,25,26). Its interval distribution resembled auditory nerve activity at this age (Fig.…”

Section: Resultsmentioning

confidence: 79%

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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Developmental Changes in Short-Term Plasticity at the Rat Calyx of Held Synapse

Cited by 50 publications

References 80 publications

Natural and lesion‐induced decrease in cell proliferation in the medial nucleus of the trapezoid body during hearing development

Natural and lesion‐induced decrease in cell proliferation in the medial nucleus of the trapezoid body during hearing development

Actin-dependent rapid recruitment of reluctant synaptic vesicles into a fast-releasing vesicle pool

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

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