Short-Term Plasticity at Hippocampal Mossy Fiber Synapses Is Induced by Natural Activity Patterns and Associated with Vesicle Pool Engram Formation

Vandael, David; Borges-Merjane, Carolina; Zhang, Xiaomin; Jónás, Péter

doi:10.1016/j.neuron.2020.05.013

Cited by 94 publications

(156 citation statements)

References 79 publications

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“…Thus, MOD may be a promising technique to analyze in vivo intracellular recordings, in which signal-to-noise ratio is low (Lee et al, 2009;Pernía-Andrade and Jonas, 2014). To test whether the method was also suitable for analysis of EPSCs, we performed similar ground truth simulations in CA3 pyramidal neurons to mimic a previously recorded voltage-clamp data set (Vandael et al, 2020). As expected, the method was also able to accurately retrieve synaptic activity under these conditions of increased resolution.…”

Section: Mod Allows Efficient and Reliable Event Detection In Synthetmentioning

confidence: 92%

“…Paired recordings from hippocampal mossy fiber terminals and CA3 pyramidal neurons in hippocampal slices in vitro were performed as described previously (Bischofberger et al, 2006;Vyleta and Jonas, 2014;Vyleta et al, 2016;Vandael et al, 2020). represented as the height of the box.…”

Section: In Vitro Recordingmentioning

confidence: 99%

“…4A). Mossy fiber terminals were stimulated non-invasively with a 1-s, 100-Hz train of pulses in the cell-attached mode, while adjacent CA3 pyramidal neurons were recorded in the whole-cell voltage-clamp configuration (Bischofberger et al, 2006;Vyleta et al, 2016;Vandael et al, 2020). These recording conditions were also challenging for MOD, because EPSC frequency was enhanced during and after high-frequency stimulation (Fig.…”

Section: Mod Improves Epsc Detection In In Vitro Data Setsmentioning

confidence: 99%

“…For GCs, specific membrane resistance was set to Rm = 38,000  cm 2 , specific membrane capacitance to Cm = 1 µF cm -2 , and axial resistance to Ri = 194  cm (Schmidt-Hieber et al, 2007). For CA3 pyramidal neurons, specific membrane resistance was set to Rm = 113,000  cm 2 , specific membrane capacitance to Cm = 1.13 µF cm -2 , axial resistance to Ri = 268  cm (Major et al, 1994; Rm and Cm were scaled by a factor of 1.5 to account for the high density of spines in CA3 pyramidal neurons); access resistance was set to 6.9 M (Vandael et al, 2020).…”

mentioning

confidence: 99%

“…For GCs, current-clamp recordings of EPSPs were simulated to mimic conditions of a previously recorded in vivo data set (Zhang et al, 2020). For CA3 pyramidal neurons, voltageclamp recordings of EPSCs were simulated to replicate conditions of a previous paired recording data set (Vandael et al, 2020).…”

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confidence: 99%

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MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic eventsin vivo

Zhang

Schloegl

Vandael

et al. 2020

Preprint

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AbstractTo understand the mechanisms of information coding in single neurons, it is necessary to analyze subthreshold synaptic events, action potentials (APs), and the interrelation between these two forms of activity in different behavioral states. However, detecting excitatory postsynaptic potentials (EPSPs) or currents (EPSCs) in awake, behaving animals remains challenging, because of unfavorable signal-to-noise ratio, high frequency, fluctuating amplitude, and variable time course of synaptic events. Here, we developed a new method for synaptic event detection, termed MOD (Machine-learning Optimal-filtering Detection-procedure), which combines concepts of supervised machine learning and optimal Wiener filtering. First, experts were asked to manually score short epochs of data. Second, the algorithm was trained to obtain the optimal filter coefficients of a Wiener filter and the optimal detection threshold. Third, scored and unscored data were processed with the optimal filter, and events were detected as peaks above threshold. Finally, the area under the curve (AUC) of the receiver operating characteristics (ROC) curve was used to quantify accuracy and efficiency of detection. Additionally, cross-validation was performed to exclude overfitting of the scored data, a potential concern with machine-learning approaches. We then challenged the new detection method with EPSP traces in vivo in mice during spatial navigation and EPSC traces in vitro in slices under conditions of enhanced transmitter release. When benchmarked using a (1−AUC)−1 metric, MOD outperformed previous methods (template-fit and deconvolution) by a factor of up to 3. Thus, MOD may become an important tool for large-scale analysis of synaptic activity in vivo and in vitro.HighlightsA new method for detection of synaptic events, termed MOD, is describedThe method combines the concepts of supervised machine learning and optimal filteringThe method is useful for analysis of both in vitro and in vivo data setsMOD outperforms previously published methods for synaptic event detection by a factor of up to 3

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Section: Mod Allows Efficient and Reliable Event Detection In Synthetmentioning

confidence: 92%

Section: In Vitro Recordingmentioning

confidence: 99%

Section: Mod Improves Epsc Detection In In Vitro Data Setsmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic eventsin vivo

Zhang

Schloegl

Vandael

et al. 2020

Preprint

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The unique plasticity of hippocampal adult‐born neurons: Contributing to a heterogeneous dentate

Huckleberry

Shansky

2021

Hippocampus

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The dentate gyrus (DG) of the hippocampus is evolutionarily conserved as one of the few sites of adult neurogenesis in mammals. Although there is clear evidence that neurogenesis is necessary for healthy hippocampal function, whether adult-born neurons are simply integrated into existing hippocampal networks to serve a similar purpose to that of developmentally born neurons or whether they represent a discrete cell population with unique functions remains less clear. In this review, we consider evidence for discrete cellular, synaptic, and structural features of adult-born DG neurons, suggesting that neurogenesis contributes to the formation of a heterogeneous DG. We therefore propose that hippocampal neurogenesis creates a specialized neuronal subpopulation that may play a key role in hippocampal functions like episodic memory. We note critical gaps in this extensive body of work, including a general failure to include female animals in relevant research and a need for more precise consideration of intrahippocampal neuroanatomy.

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Unc13A dynamically stabilizes vesicle priming at synaptic release sites for short-term facilitation and homeostatic potentiation

Jusyte,

Blaum,

Böhme

et al. 2023

Cell Reports

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Short-Term Plasticity at Hippocampal Mossy Fiber Synapses Is Induced by Natural Activity Patterns and Associated with Vesicle Pool Engram Formation

Cited by 94 publications

References 79 publications

MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic eventsin vivo

MOD: A novel machine-learning optimal-filtering method for accurate and efficient detection of subthreshold synaptic eventsin vivo

The unique plasticity of hippocampal adult‐born neurons: Contributing to a heterogeneous dentate

Unc13A dynamically stabilizes vesicle priming at synaptic release sites for short-term facilitation and homeostatic potentiation

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