Target‐cell‐dependent plasticity within the mossy fibre–CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites

Pelkey, Kenneth A.; McBain, Chris J.

doi:10.1113/jphysiol.2007.148635

Cited by 51 publications

(44 citation statements)

References 68 publications

(101 reference statements)

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“…This is consistent with previous studies at excitatory and inhibitory synapses (Ali and Nelson 2006;Poncer et al 1997). The present study is also consistent with previous studies reporting P/Q-type, but not N-type, channels mediate GABA release from fast-spiking interneurons to pyramidal cells (Zaitsev et al 2007;Hefft and Jonas 2005), since the CCK-negative interneurons here displayed fast IPSPs, insensitive to CB1 pharmacology.…”

Section: Discussionsupporting

confidence: 82%

“…Evidence suggests that specific calcium channels are selectively associated with specific types of synaptic connections (Poncer et al 1997;Ali and Nelson 2006). It is unknown whether the same type of presynaptic calcium channels type is associated with specific short-term dynamics at interneuron-interneuron connections.…”

Section: Cck-negative Quadrilaminar Cells In Slmmentioning

confidence: 99%

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CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1

Ali

2011

Journal of Neurophysiology

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Ali AB. CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1. J Neurophysiol 105: 1051-1062, 2011. First published December 1, 2010; doi:10.1152/jn.00831.2010.-One of the critical factors in determining network behavior of neurons is the influence of local circuit connections among interneurons. The short-term synaptic plasticity and the subtype of presynaptic calcium channels used at local circuit connections of inhibitory interneurons in CA1 were investigated using dual whole-cell recordings combined with biocytin and double immunofluorescence labeling in acute slices of P18-to 21-day-old rat stratum radiatum (SR) and stratum lacunosum moleculare (SLM). Two forms of temporally distinct synaptic facilitation were observed among interneuron connections involving presynaptic cholecystokinin (CCK)-positive cells in SR, frequency-dependent facilitation, and a delayed onset of release (45-80 ms) with subsequent facilitation (DORF). Inhibition at both these synapses was under tonic cannabinoid-type 1 (CB1) receptor activity. DORF synapses did not display conventional release-dependent properties; however, blocking CB1 receptors with antagonist AM-251 (10 M) altered the synaptic transmission to frequency-dependent depression with a fast onset of release (2-4 ms). Presynaptic CCK-negative interneurons in SLM elicited inhibitory postsynaptic potentials (IPSPs) insensitive to CB1 receptor pharmacology displayed frequency-dependent depression. Release of GABA at facilitating synapses was solely mediated via N-type presynaptic calcium channels, whereas depressing synapses utilized P/Q-type channels. These data reveal two distinct models of neurotransmitter release patterns among interneuron circuits that correlate with the subtype of presynaptic calcium channel. These data suggest that endocannabinoids act via CB1 receptors to selectively modulate N-type calcium channels to alter signal transmission.cannabinoid type 1 receptors; cholecystokinin; short-term plasticity GABAERGIC INTERNEURONS ARE important in generating rhythmic activity by creating regular and temporally coordinated spike timing and synaptic integration in populations of neurons (Mann et al. 2005;Miles et al. 1996). The diverse subclasses of interneurons are characterized by criteria such as neurochemical marker expression, dendritic and axonal morphology, and electrophysiological properties Freund and Buzsaki 1996). Anatomical studies reveal the existence of various subclasses of interneurons in stratum radiatum (SR) and stratum lacunosum moleculare (SLM) of CA1 Freund and Buzsaki 1996). Although these two subregions are rich in different subclasses of interneurons, the physiology and pharmacological properties of the connections among these various subclasses of interneurons need further investigation. Physiologically, it has been shown that subclasses of interneurons in stratum pyramidale (SP) and stratum oriens contribute differentially to network oscillations at distinct ...

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Section: Discussionsupporting

confidence: 82%

Section: Cck-negative Quadrilaminar Cells In Slmmentioning

confidence: 99%

CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1

Ali

2011

Journal of Neurophysiology

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“…A striking example of such topographic specialization is the axonal arbour, which is typically complex and often conveys information to widely distributed brain regions. Individual axonal branches within a single arbour can exhibit distinct morphologies, synaptic release properties and activity-dependent structural and functional regulation (1). A fundamental question is how such morphological and functional diversity is achieved, modified and maintained within a complex axonal arbour controlled by a single soma.…”

Section: Introductionmentioning

confidence: 99%

Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains

et al. 2017

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Local mRNA translation in growing axons allows for rapid and precise regulation of protein expression in response to extrinsic stimuli. However, the role of local translation in mature CNS axons is unknown. Such a mechanism requires the presence of translational machinery and associated mRNAs in circuit-integrated brain axons. Here we use a combination of genetic, quantitative imaging and super-resolution microscopy approaches to show that mature axons in the mammalian brain contain ribosomes, the translational regulator FMRP and a subset of FMRP mRNA targets. This axonal translational machinery is associated with Fragile X granules (FXGs), which are restricted to axons in a stereotyped subset of brain circuits. FXGs and associated axonal translational machinery are present in hippocampus in humans as old as 57 years. This FXGassociated axonal translational machinery is present in adult rats, even when adult neurogenesis is blocked. In contrast, in mouse this machinery is only observed in juvenile hippocampal axons. This differential developmental expression was specific to the hippocampus, as both mice and rats exhibit FXGs in mature axons in the adult olfactory system. Experiments in Fmr1 null mice show that FMRP regulates axonal protein expression but is not required for axonal transport of ribosomes or its target mRNAs. Axonal translational machinery is thus a feature of adult CNS neurons. Regulation of this machinery by FMRP could support complex behaviours in humans throughout life.

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“…Namely, the unusually large (3-6 m; so-called "giant") MF terminals innervate primarily pyramidal cells, whereas small filopodia emanating from the giant terminals and small en passant boutons contact GABAergic cells (Acsády et al, 1998). Since single MFs contact more GABAergic targets (30 -50) than do CA3 pyramidal cells (10 -20) [note that these uniquely low numbers indicate the unusual sparsity of the synaptic outputs from single granule cells (Acsády et al, 1998)], the excitation of GABAergic cells by granule cells is likely to be a significant regulator of the output of CA3 pyramidal cells Lawrence and McBain, 2003;Mori et al, 2004Mori et al, , 2007Pelkey and McBain, 2008). However, the types of CA3 GABAergic cells targeted by MFs and the physiological properties of MF inputs onto distinct types of GABAergic cells are not well understood.…”

Section: Introductionmentioning

confidence: 99%

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

Szabadics¹,

Soltész²

2009

J. Neurosci.

105

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One million mossy fibers in the rat provide individually sparse but functionally important synaptic connections between the dentate gyrus and hippocampus. Although the majority of mossy fiber targets are GABAergic cells, the functional organization of the feedforward GABAergic machinery modulating the interactions of granule cells and CA3 pyramidal cells are not yet understood. We used mossy fiber bouton to GABA neuron paired recordings in the CA3 to demonstrate that mossy fibers provide cell type-specific innervation to distinct GABAergic neurons with specialized intra-and extrahippocampal outputs. Our results show that mossy fibers contact the perisomatically projecting fast-spiking and regular-spiking basket cells, in addition to the dendritically projecting ivy cells, and the septum-projecting spiny stratum lucidum cells. Monosynaptic mossy fiber inputs to fast-spiking basket cells and spiny stratum lucidum cells were found to be numerous, but they were small in amplitude and displayed low transmission probabilities. In contrast, regular-spiking basket cells and ivy cells were less likely to be innervated by mossy fibers, but the amplitudes of mossy fiber EPSCs were large and the transmission probabilities were high. The dependence of the numbers and strengths of the mossy fiber inputs to CA3 GABAergic cells on the postsynaptic cell type was correlated with the frequency of the background synaptic events, so that cells with weak but numerous mossy fiber inputs received high rates of spontaneous synaptic events. Together, these results reveal the diverse components and high degree of functional specificity of the GABAergic cellular machinery underlying the dentate gyrus-CA3 interface.

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Target‐cell‐dependent plasticity within the mossy fibre–CA3 circuit reveals compartmentalized regulation of presynaptic function at divergent release sites

Cited by 51 publications

References 68 publications

CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1

CB1 modulation of temporally distinct synaptic facilitation among local circuit interneurons mediated by N-type calcium channels in CA1

Axonal ribosomes and mRNAs associate with fragile X granules in adult rodent and human brains

Functional Specificity of Mossy Fiber Innervation of GABAergic Cells in the Hippocampus

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