Target-Dependent Feedforward Inhibition Mediated by Short-Term Synaptic Plasticity in the Cerebellum

Bao, Jin; Reim, Kerstin; Sakaba, Takeshi

doi:10.1523/jneurosci.0276-10.2010

Cited by 78 publications

(86 citation statements)

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“…Target-specific regulation of STP has also been documented in neocortical, hippocampal, and cerebellar preparations (Bao et al 2010;Koester and Johnston 2005;Markram et al 1998;Reyes et al 1998;Scanziani et al 1998;Sun et al 2005;Sylwestrak and Ghosh 2012 Shigemoto et al 1996;Sun et al 2009;Sylwestrak and Ghosh 2012;Tomioka et al 2014;Vitureira et al 2011). The finding reported here that release probability across fibers is specified in a target-dependent manner suggests that release probability, and short-term synaptic dynamics, is important for the auditory information transmission at the nerve-to-cochlear nucleus connection.…”

Section: Convergent Afferents Show Target-dependent Synaptic Plasticitysupporting

confidence: 56%

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

Ahn

MacLeod

2016

Journal of Neurophysiology

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Ahn J, MacLeod KM. Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus. J Neurophysiol 115: 1679 -1690, 2016. First published December 30, 2015 doi:10.1152/jn.00752.2015.-Short-term synaptic plasticity (STP) acts as a time-and firing rate-dependent filter that mediates the transmission of information across synapses. In the auditory brain stem, the divergent pathways that encode acoustic timing and intensity information express differential STP. To investigate what factors determine the plasticity expressed at different terminals, we tested whether presynaptic release probability differed in the auditory nerve projections to the two divisions of the avian cochlear nucleus, nucleus angularis (NA) and nucleus magnocellularis (NM). Estimates of release probability were made with an openchannel blocker of N-methyl-D-aspartate (NMDA) receptors. Activity-dependent blockade of NMDA receptor-mediated excitatory postsynaptic currents (EPSCs) with application of 20 M (ϩ)-MK801 maleate was more rapid in NM than in NA, indicating that release probability was significantly higher at terminals in NM. Paired-pulse ratio (PPR) was tightly correlated with the blockade rate at terminals in NA, suggesting that PPR was a reasonable proxy for relative release probability at these synapses. To test whether release probability was similar across convergent inputs onto NA neurons, PPRs of different nerve inputs onto the same postsynaptic NA target neuron were measured. The PPRs, as well as the plasticity during short trains, were tightly correlated across multiple inputs, further suggesting that release probability is coordinated at auditory nerve terminals in a target-specific manner. This highly specific regulation of STP in the auditory brain stem provides evidence that the synaptic dynamics are tuned to differentially transmit the auditory information in nerve activity into parallel ascending pathways.short-term plasticity; depression; angularis; release probability; magnocellularis

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Section: Convergent Afferents Show Target-dependent Synaptic Plasticitysupporting

confidence: 56%

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

Ahn

MacLeod

2016

Journal of Neurophysiology

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“…Synapses where facilitation and depression are both present can act as band pass filters (Dittman et al, 2000). In addition, a single neuron can contact multiple postsynaptic partners using synapses with different forms of short-term plasticity, suggesting that short-term plasticity is tuned in a target-dependent manner (Bao et al, 2010; Maccaferri et al, 1998; Markram et al, 1998; Reyes et al, 1998; Rozov et al, 2001; Scanziani et al, 1998; Sherman and Atwood, 1972). Short-term plasticity could also be important for the induction of long-term forms of plasticity.…”

Section: Theorized Roles Of Facilitationmentioning

confidence: 99%

The Mechanisms and Functions of Synaptic Facilitation

Jackman

Regehr

2017

Neuron

383

338

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Summary The ability of the brain to store and process information relies on changing the strength of connections between neurons. Synaptic facilitation is a form of short-term plasticity that enhances synaptic transmission for less than a second. Facilitation is a ubiquitous phenomenon thought to play critical roles in information transfer and neural processing. Yet our understanding of the function of facilitation remains largely theoretical. Here we review proposed roles for facilitation, and discuss how recent progress in uncovering the underlying molecular mechanisms could enable experiments that elucidate how facilitation, and short-term plasticity in general, contribute to circuit function and animal behavior.

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“…Most synapses show short-term plasticity (Klug et al, 2012;Regehr, 2012;Blackman et al, 2013). In oscillatory networks, shortterm plasticity allows synapses to exhibit frequency-dependent efficacy (Nadim and Manor, 2000;Fortune and Rose, 2001;Abbott and Regehr, 2004;Bao et al, 2010) by adjusting the synaptic strength in response to input frequency (Rothman et al, 2009;Regehr, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…In oscillatory networks, shortterm plasticity allows synapses to exhibit frequency-dependent efficacy (Nadim and Manor, 2000;Fortune and Rose, 2001;Abbott and Regehr, 2004;Bao et al, 2010) by adjusting the synaptic strength in response to input frequency (Rothman et al, 2009;Regehr, 2012). The most common forms of short-term plasticity are depression and facilitation (Fioravante and Regehr, 2011), but synapses often demonstrate both, resulting in a preferred presynaptic frequency at which the synapse responds with maximal efficacy (Markram et al, 1998;Izhikevich et al, 2003;Drover et al, 2007;Oh et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

The Frequency Preference of Neurons and Synapses in a Recurrent Oscillatory Network

Tseng

Martínez

Nadim

2014

Journal of Neuroscience

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A variety of neurons and synapses shows a maximal response at a preferred frequency, generally considered to be important in shaping network activity. We are interested in whether all neurons and synapses in a recurrent oscillatory network can have preferred frequencies and, if so, whether these frequencies are the same or correlated, and whether they influence the network activity. We address this question using identified neurons in the pyloric network of the crab Cancer borealis. Previous work has shown that the pyloric pacemaker neurons exhibit membrane potential resonance whose resonance frequency is correlated with the network frequency. The follower lateral pyloric (LP) neuron makes reciprocally inhibitory synapses with the pacemakers. We find that LP shows resonance at a higher frequency than the pacemakers and the network frequency falls between the two. We also find that the reciprocal synapses between the pacemakers and LP have preferred frequencies but at significantly lower values. The preferred frequency of the LP to pacemaker synapse is correlated with the presynaptic preferred frequency, which is most pronounced when the peak voltage of the LP waveform is within the dynamic range of the synaptic activation curve and a shift in the activation curve by the modulatory neuropeptide proctolin shifts the frequency preference. Proctolin also changes the power of the LP neuron resonance without significantly changing the resonance frequency. These results indicate that different neuron types and synapses in a network may have distinct preferred frequencies, which are subject to neuromodulation and may interact to shape network oscillations.

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Target-Dependent Feedforward Inhibition Mediated by Short-Term Synaptic Plasticity in the Cerebellum

Abstract: Cerebellar feedforward inhibition (FFI) is mediated by two distinct pathways targeting different subcellular compartments of Purkinje cells (PCs

Cited by 78 publications

References 50 publications

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

Target-specific regulation of presynaptic release properties at auditory nerve terminals in the avian cochlear nucleus

The Mechanisms and Functions of Synaptic Facilitation

The Frequency Preference of Neurons and Synapses in a Recurrent Oscillatory Network

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