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

Ali, Afia B.

doi:10.1152/jn.00831.2010

Cited by 12 publications

(17 citation statements)

References 43 publications

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“…One can explain the presynaptic dependency of I→E and I→I dynamics by similar mechanisms. Indeed, differences in the subtypes of Ca 2+ channels in presynaptic terminals have been implicated in a study of facilitating and depressing synapses made, respectively, by cholecystokinin (CCK)-positive and CCK-negative interneurons in the hippocampus (Ali, 2011). …”

Section: Discussionmentioning

confidence: 99%

Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype

Ma¹,

Hu²,

Agmon³

2012

J. Neurosci.

110

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Excitatory-to-inhibitory cortical synapses exhibit either short-term facilitation or depression, depending on the subtype identity of the postsynaptic interneuron, while the short-term plasticity (STP) of inhibitory-to-excitatory synapses depends on the presynaptic interneuron. However, the rules governing STP of inhibitory-to-inhibitory synapses have not yet been determined. We recorded 109 unitary connections made by the two major inhibitory interneuron subtypes in layer 4 of mouse somatosensory cortex, fast-spiking (FS) and somatostatin-containing (SOM) interneurons, on each other and on excitatory, regular-spiking (RS) neurons. In all pairs we measured dynamic changes in the postsynaptic response to a 20 Hz train of presynaptic action potentials. In half of our dataset, we also measured kinetic properties of the unitary IPSC: latency, rise-time and decay time-constant. We found a pronounced dependency of STP on the presynaptic, but not the postsynaptic identity: FS interneurons made strongly depressing connections on FS, SOM and RS targets, while in synapses made by SOM interneurons on FS and RS targets, weak early depression was followed by weak late facilitation. IPSC latency and rise-time were also strongly dependent on the presynaptic interneuron subtype, being 1.5–2x slower in output synapses of SOM, compared to FS interneurons. In contrast, the IPSC decay time-constant depended only on the postsynaptic class, with 1.5x slower decay on excitatory, compared to inhibitory targets. The properties of the inhibitory outputs of FS and SOM interneurons reciprocate the properties of their excitatory inputs, and imply a dynamic spatio-temporal division of labor between these two major inhibitory subsystems.

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Section: Discussionmentioning

confidence: 99%

Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype

Ma¹,

Hu²,

Agmon³

2012

J. Neurosci.

110

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“…Carbachol may enhance DSI by stimulating the firing of cholecystokinin‐positive GABA neurons (Kawaguchi, 1997; Cea‐del Rio et al 2010) that are the main source of cannabinoid‐sensitive synapses (Glickfeld & Scanziani, 2006; Neu et al 2007; Galarreta et al 2008; Lee et al 2010; Ali, 2011). However, synapses from some cholecystokinin‐positive cells onto pyramidal neurons are cannabinoid‐insensitive (Lee et al 2010; Ali, 2011) possibly because they lack CB1Rs (Eggan et al 2010). Moreover, carbachol also stimulates somatostatin‐ and vasoactive intestinal peptide‐positive GABA neurons (Kawaguchi, 1997; Fanselow et al 2008), which are not thought to provide cannabinoid‐sensitive synapses, although somatostatin neurons contain CB1R mRNA (Hill et al 2007).…”

Section: Discussionmentioning

confidence: 99%

“…Carbachol may enhance DSI by stimulating the firing of cholecystokinin-positive GABA neurons (Kawaguchi, 1997;Cea-del Rio et al 2010) that are the main source of cannabinoid-sensitive synapses (Glickfeld & Scanziani, 2006;Neu et al 2007;Galarreta et al 2008;Lee et al 2010;Ali, 2011). However, synapses from some cholecystokinin-positive cells onto pyramidal neurons are cannabinoid-insensitive Ali, 2011) possibly because they lack CB1Rs .…”

Section: Figure 10 Daglα Deficiency Abolishes Dsi Induced By Action mentioning

confidence: 99%

Postsynaptic diacylglycerol lipase α mediates retrograde endocannabinoid suppression of inhibition in mouse prefrontal cortex

Yoshino

Miyamae

Hansen

et al. 2011

The Journal of Physiology

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Non-technical summary In multiple brain regions, endogenous cannabinoids suppress inhibitory synaptic transmission; however, the biochemical/molecular pathways for endocannabinoid synthesis are poorly understood. Endocannabinoid signalling may be crucial for microcircuit function in the prefrontal cortex (PFC), a cortical region involved in complex behaviours. However, endocannabinoid signalling remains largely unexplored in the PFC. Using enzymatic inhibitors, we show that modulation of inhibitory synaptic transmission in PFC neurons is mediated by the endocannabinoid 2-arachidonoylglycerol synthesized postsynaptically. Interestingly, diacylglycerol lipase (DAGL), the 2-arachidonoylglycerol synthesis enzyme, has two isoforms: DAGLα and DAGLβ. Studying PFC neurons from DAGLα −/− , DAGLβ −/− and wild-type mice, we show that only DAGLα is involved in the suppression of inhibitory transmission in the PFC.Abstract Depolarization-induced suppression of inhibition (DSI) is a prevailing form of endocannabinoid signalling. However, several discrepancies have arisen regarding the roles played by the two major brain endocannabinoids, 2-arachidonoylglycerol (2-AG) and anandamide, in mediating DSI. Here we studied endocannabinoid signalling in the prefrontal cortex (PFC), where several components of the endocannabinoid system have been identified, but endocannabinoid signalling remains largely unexplored. In voltage clamp recordings from mouse PFC pyramidal neurons, depolarizing steps significantly suppressed IPSCs induced by application of the cholinergic agonist carbachol. DSI in PFC neurons was abolished by extra-or intracellular application of tetrahydrolipstatin (THL), an inhibitor of the 2-AG synthesis enzyme diacylglycerol lipase (DAGL). Moreover, DSI was enhanced by inhibiting 2-AG degradation, but was unaffected by inhibiting anandamide degradation. THL, however, may affect other enzymes of lipid metabolism and does not selectively target the α (DAGLα) or β (DAGLβ) isoforms of DAGL. Therefore, we studied DSI in the PFC of DAGLα −/− and DAGLβ −/− mice generated via insertional mutagenesis by gene-trapping with retroviral vectors. Gene trapping strongly reduced DAGLα or DAGLβ mRNA levels in a locus-specific manner. In DAGLα −/− mice cortical levels of 2-AG were significantly decreased and DSI was completely abolished, whereas DAGLβ deficiency did not alter cortical 2-AG levels or DSI. Importantly, cortical levels of anandamide were not significantly affected in DAGLα −/− or DAGLβ −/− mice. The chronic decrease of 2-AG levels in DAGLα −/− mice did not globally alter inhibitory transmission or the response of cannabinoid-sensitive synapses to cannabinoid receptor stimulation, although it altered some intrinsic membrane properties. synaptic inhibition in a DAGLα-dependent manner. These results show that DSI is a prominent form of endocannabinoid signalling in PFC circuits. Moreover, the close agreement between our pharmacological and genetic studies indicates that 2-AG synthesized by postsynaptic DAGLα mediates DSI in P...

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“…Cell pairs used in the simulations were pulled out from a data-driven reconstruction of the rat 215 CA1 region, built with the pipeline presented in Markram et al (2015). Number of synapses per 216 connection for experimentally characterized pathways (Ali, 2011;Biro et al, 2005;Buhl et al, 217 1994a,b;Deuchars and Thomson, 1996;Földy et al, 2010;Maccaferri et al, 2000;Sik et al, 218 1995;Vida et al, 1998) (r = 0.98, Figure 2 b and Supplementary Table S3) along with targeting 219 profile (Figure 2 a) was verified for this work. PSP attenuation in the active dendrites of PCs 220 (Migliore et al, 2018) is also in line with the experimentally reported curves (Magee and Cook,221 2000) (Supplementary Figure S1).…”

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confidence: 61%

Data-driven integration of hippocampal CA1 synapse physiology in silico

Ecker

Romani

Sáray

et al. 2019

Preprint

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1The anatomy and physiology of synaptic connections in rodent hippocampal CA1 have been 2 exhaustively characterized in recent decades. Yet, the resulting knowledge remains disparate 3 and difficult to reconcile. Here, we present a data-driven approach to integrate the current 4 state-of-the-art knowledge on the synaptic anatomy and physiology of rodent hippocampal CA1, 5 including axo-dendritic innervation patterns, number of synapses per connection, quantal con-6 ductances, neurotransmitter release probability, and short-term plasticity into a single coherent 7 resource. First, we undertook an extensive literature review of paired-recordings of hippocam-8 pal neurons and compiled experimental data on their synaptic anatomy and physiology. The 9 data collected in this manner is sparse and inhomogeneous due to the diversity of experimental 10 techniques used by different labs, which necessitates the need for an integrative framework to 11 unify these data. To this end, we extended a previously developed workflow for the neocortex to 12 constrain a unifying in silico reconstruction of the synaptic physiology of CA1 connections. Our 13 work identifies gaps in the existing knowledge and provides a complementary resource towards 14 a more complete quantification of synaptic anatomy and physiology in the rodent hippocampal 15 CA1 region. 17The hippocampal CA1 region is probably the most studied region of the mammalian brain and 20 is thought to play a pivotal role in learning and memory (Bliss and Collingridge, 2013; Buzsáki, 21 1989). Neuronal microcircuits in the hippocampal CA1 region process and store information 22 through a myriad of cell-type-specific synaptic connections. Previous studies have identified that 23 hippocampal cell-types are connected through multiple synapses, which are positioned across 24 distinct axo-dendritic domains with a diversity of short-and long-term dynamics, as well as 25 synaptic strengths. Despite the wealth of data, we lack an integrative framework to reconcile the 26 diversity of synaptic physiology, and therefore, identify knowledge gaps. There have been several 27 1 Ecker et al.Integration of CA1 synapse physiology in silico recent attempts to integrate knowledge about the hippocampal CA1 (Bezaire and Soltesz, 2013; 28 Wheeler et al., 2015), however, they were not focused on the dynamics of synaptic transmission. 29Recent attempts have extended the utility of the online resource hippocampome.org towards 30 synaptic electrophysiology as well (Moradi and Ascoli, 2019). However, in the continuing spirit 31 of hippocampome.org, the study is primarily a text mining-based collection of papers and pa-32 rameters, which does not integrate these data into a unifying framework. As a way forward, 33 we extended a previously developed workflow to integrate disparate data on the physiology of 34 synaptic transmission in hippocampal CA1, identified and extrapolated organizing principles to 35 predict knowledge gaps (Markram et al., 2015). We accounted for the dynamic and probabili...

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

Cited by 12 publications

References 43 publications

Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype

Short-Term Plasticity of Unitary Inhibitory-to-Inhibitory Synapses Depends on the Presynaptic Interneuron Subtype

Postsynaptic diacylglycerol lipase α mediates retrograde endocannabinoid suppression of inhibition in mouse prefrontal cortex

Data-driven integration of hippocampal CA1 synapse physiology in silico

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