Modulating Excitation Through Plasticity At Inhibitory-Books Pdf

Modulating excitation through plasticity at inhibitory
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Chevaleyre and Piskorowski Modulating excitation through inhibitory plasticity. FIGURE 1 Modulation and roles of GABA release from CCK receptors GABAB receptors and kainate receptors The decrease in GABA. interneurons CCK interneurons target pyramidal cell soma basket cell release differently impacts excitatory synapses depending on which subset. BS or dendrites Schaffer collateral associated cell SC A and lacunosum of CCK interneuron synapses are depressed A decrease in. moleculare radiatum perforant path associated cell LM R PP A see dendritic targeting CCK synapse facilitates LTP induction at SC CA1. Somogyi and Klausberger 2005 The release of GABA from CCK cell synapses and increases the ability of an excitatory post synaptic potential. terminals is mediated by N type calcium channels which provide a loose EPSP to evoke an action potential E S coupling When GABA release at. coupling between calcium influx and exocytosis and partially underlie the somatic targeting CCK synapses is depressed a large increase in the. asynchronous release of GABA by these cells GABA release is negatively amplitude of the SC EPSPs is observed but distal perforant path PP. controlled by the activation of several receptors CB1 cannabinoid EPSPs are unaltered. trilaminar cells show asynchronous release Daw et al 2009 receptors powerfully decreases GABA release from CCK cells. In contrast PV interneuron axon terminals express P Q type Neu et al 2007 Furthermore CCK cells are likely the only. Ca2 channels which are more tightly coupled to vesicle fusion class of interneurons expressing CB1R Marsicano and Lutz 1999. because of their location in the active zone As a consequence Tak cs et al 2014. PV interneurons have more synchronous release of GABA Hefft The exclusive modulation of one type of interneuron can have. and Jonas 2005 interesting functional consequences For example in fast spiking. CCK itself which is co released with GABA can modulate PV basket cells mu opioid receptor activation hyperpolarizes. GABA release by both CCK and PV neurons F ldy et al the membrane and depresses GABA release while nearby CCK. 2007 In CCK cells CCK release activates CCK2 receptors on basket cells are unaffected by the mu opioid receptor activa. pyramidal cells resulting in retrograde endocannabinoid release tion but are uniquely modulated by cannabinoid application. and pre synaptic activation of cannabinoid type 1 receptors Glickfeld et al 2008 Likewise a comparison of the action of. CB1R and reducing GABA release F ldy et al 2007 Karson acetylcholine on different soma targeting PV and CCK basket. et al 2008 In contrast activation of CCK2 receptors on PV cells revealed that GABA release was diminished by M2 type. basket cells results in the activation of a pertussis toxin sensitive muscarinic receptor activation uniquely in PV cells whereas. G protein Gi o coupled pathway that results in intracellular CCK cell transmission was inhibited via cannabinoid signaling. calcium release transient receptor potential TRP channel acti Szab et al 2010 Thus even though these interneuron classes. vation and membrane depolarization Lee et al 2011 This receive similar inputs and have similar axonal arbors their prop. membrane depolarization results in increased GABA release erties endow them with very different frequency tuning properties. Interestingly PV bi stratified cells showed no response to CCK and are likely active at different times Glickfeld and Scanziani. indicating that this modulation is specific to somatic inhibition 2006 Furthermore the distinct modulation of these different. and may be an important complementary component to the perisomatic interneurons can act to shift pyramidal cells into. CCK cell modulation by CCK different modes of integration. GABA release by CCK cells is uniquely altered by several. modulators For instance the synchronous release of GABA. can be decreased by presynaptic kainate receptors Daw et al CONSEQUENCES OF CCK INTERNEURON PLASTICITY ON. 2010 In addition the GABAB receptor is detected in CCK EXCITATORY CELL TRANSMISSION. cells but not in PV interneurons Sloviter et al 1999 and The CB1R is one of the most highly expressed G protein coupled. there is experimental evidence suggesting that activation of these receptors in the nervous system Herkenham et al 1990 These. Frontiers in Cellular Neuroscience www frontiersin org March 2014 Volume 8 Article 93 2. Chevaleyre and Piskorowski Modulating excitation through inhibitory plasticity. FIGURE 2 Modulation and roles of GABA release from PV release The release of GABA at PV cell synapses is negatively controlled. interneurons PV interneurons target either the soma basket cell BS by diverse receptors including mu and delta opioid receptors MOR and. the axon axo axonic cell AA or the dendrites bistratified cell BS and DOR and muscarinic M2 receptors Conversely GABA release from PV. oriens lacunosum moleculare cell OLM of pyramidal cells see Somogyi cells is increased by activation of the Neuregulin 1 receptor ErbB4 LTP. and Klausberger 2005 The release of GABA from PV cell terminals is induction at SC CA1 synapses is impaired following ErB4 activation in. mediated by P Q type calcium channels The tight coupling between PV cells due to increased pre synaptic GABA release by PV cells. calcium influx and exocytosis machinery results in precisely timed vesicle. receptors are involved in the action of endogenous cannabinoids and the active zone proteins RIM1 and Rab3b are needed for. eCBs which are synthetized from membrane lipid precursors by iLTD induction Chevaleyre et al 2007 Tsetsenis et al 2011. the postsynaptic cell and act as retrograde messengers to depress indicating that iLTD results in a change on the release machinery. transmitter release from presynaptic terminals for a general Because of the specific expression of CB1R in CCK cells eCB. review see Chevaleyre et al 2006 All of the CB1 dependant mediated plasticity initially offered a useful tool to dissect out the. plasticity discussed below are known to occur in CCK interneu role of CCK cells in controlling excitatory transmission Several. rons however it should be noted that not all CCK interneurons studies reported that the decrease in GABA release from CCK. express CB1 receptors cells could facilitate LTP induction at the Schaffer collateral SC. In the hippocampus eCBs are involved in two forms of CA1 excitatory synapse Not surprisingly the time course of the. synaptic plasticity When transiently released for instance by facilitation follows the time course of the eCB mediated plasticity. depolarization of the postsynaptic cell they mediate a short For instance it was initially described that the dis inhibition. term 1 min depression of GABA release a phenomenon occurring during DSI provides a transient facilitation of LTP. called depolarization induced suppression of inhibition DSI induction at excitatory synapses Carlson et al 2002 In contrast. This phenomenon was initially described more than 20 years ago induction of iLTD by eCB provides a long lasting facilitation. in the cerebellum Llano et al 1991 and hippocampus Pitler on the induction of eLTP Chevaleyre and Castillo 2004 Zhu. and Alger 1992 The retrograde action of eCBs was attributed and Lovinger 2007 The spatial localization of the facilitation. by Wilson and Nicoll 2001 The fast onset of DSI and the lack depends on the induction protocol used to evoke eCB release. of sensitivity of tetrodotoxin TTX resistant miniature IPSCs to DSI is a single cell phenomenon thus eLTP facilitation will only. DSI Alger et al 1996 are in agreement with a direct block of occur onto the cell expressing DSI However DSI targets multiple. N type Ca2 channels by subunits of the G protein an effect CB1R sensitive inhibitory synapses along the somato dendritic. that was initially demonstrated in expression systems Mackie and compartment and will likely facilitate LTP induction at excitatory. Hille 1992 inputs targeting different locations of the apical dendrite In. When a more sustained release of eCB is evoked for instance contrast iLTD can be evoked by a very localized activation of the. following activation of group I metabotropic glutamate recep Schaffer collaterals The activation of mGluR I onto pyramidal. tor mGluR I eCBs can mediate a long term depression of neurons triggers eCB release that hetero synaptically decreases. inhibitory transmission Several minutes of CB1R activation are GABA release from nearby inhibitory terminals Chevaleyre. needed for a lasting depression to be induced This more sus and Castillo 2003 Because iLTD is spatially restricted to the. tained CB1R activation probably allows for significant changes region surrounding the stimulated excitatory fibers eLTP facili. in second messenger and phosphorylation levels of downstream tation is limited to the nearby dendritic region Chevaleyre and. target molecules Consistently protein kinase A PKA activity Castillo 2004 However it was recently reported that iLTD can. Frontiers in Cellular Neuroscience www frontiersin org March 2014 Volume 8 Article 93 3. Chevaleyre and Piskorowski Modulating excitation through inhibitory plasticity. be evoked with repetitive postsynaptic firing indiscriminately been identified in a study examining five common interneuron. affecting somatic and dentritic inhibitory inputs Younts et al subtypes as defined by axonal projections and molecular expres. 2013 Therefore it is expected that facilitation of eLTP will not sion profiles Nissen et al 2010 In this work the authors found. be spatially restricted following this mode of induction that excitatory synapses express LTP onto PV basket cells and. Independently of the facilitation of eLTP described above the LTD onto bistratified cells Both of these phenomena were inde. decrease in GABA release from CCK cells can also increase the pendent of N Methyl D aspartate NMDA receptor activation. ability of an excitatory post synaptic potential EPSP to evoke an and potentially act to shift the inhibition on excitatory cells from. action potential E S coupling and directly increase the size of the dendrites to the soma A closer examination of the FF and. the EPSP at the SC CA1 synapse The first effect was observed feedback FB excitatory inputs onto PV basket cells found that. after inducing iLTD with synaptic activity of the SC inputs NMDA receptors are only found at synapses with FB afferents. or with repetitive postsynaptic depolarization Action potential leading to a narrower frequency tuning of LTP at these inputs. firing was extracellularly monitored Chevaleyre and Castillo than at FF inputs Le Roux et al 2013 Given the importance. 2003 or recorded in individual pyramidal cells Younts et al of FF inhibition to ensure the temporal fidelity of pyramidal. 2013 and was increased with both iLTD inducing protocols The cell firing Pouille and Scanziani 2001 and the very tight time. second effect i e a direct increase in the amplitude of SC EPSP lock of basket cell interneurons and pyramidal cells during sharp. was reported recently by two studies using a paired stimulation wave ripples Klausberger and Somogyi 2008 it is possible the. between proximal SC and distal perforant path PP excita different properties of LTP at FF and FB synapses is permitting. tory inputs termed input timing dependent plasticity ITDP PV cells to modulate their activity in accordance with excitation. Dudman et al 2007 The initial study showed that the pairing PV basket cells in area CA1 have recently been shown to. protocol induced a potentiation of SC EPSPs and that this poten undergo a long term increase in excitability in response to brief. tiation is dependent on eCB mediated LTD at inhibitory synapses high frequency stimulation of SC inputs Campanac et al 2013. Xu et al 2012 The dependence on CB1R strongly suggests that It was elegantly shown that this enhanced FF inhibition in area. the interneurons expressing iLTD were CCK cells This idea was CA1 was due to an increase in the inherent excitability of PV. formally demonstrated in a second thorough and elegant study cells resulting from activation of mGluR5 and subsequent down. using multiple techniques to better elucidate the phenomenon regulation of D type potassium current carried by Kv1 channels. Basu et al 2013 The authors showed that transmission from termed LTP IEPV BC The authors demonstrated that clustered. CCK interneurons is depressed following the ITDP protocol spiking in the range was increased allowing for the speculation. In addition this depression concerns perisomatic CCK termi that this plasticity may provide a use dependent modulation. nals and is mediated by eCB release during the ITDP protocol of hippocampal oscillations or even potentially allow for a. Finally they showed that most of the increase in EPSP amplitude modulation of the phase lag of PV basket cells during activity. following the ITDP protocol is the result of the eCB mediated PV interneurons may be playing an interesting role in medi. iLTD at CCK terminals These studies convincingly show that ating the ability of CA3 neurons to excite CA2 pyramidal cells. CCK interneurons targeting the soma of pyramidal neurons are A very strong FF inhibition at the SC CA2 synapse induces a. playing an important role in controlling the strength of SC inputs very large hyperpolarization in CA2 pyramidal neurons and com. These data therefore suggest that CCK interneurons should con pletely prevents SC axons from driving firing in CA2 pyramidal. tribute significantly to the feed forward FF inhibition evoked neurons Chevaleyre and Siegelbaum 2010 Kohara et al 2014. inhibitory transmission it had become evident that inhibitory synapses are not only plastic but also provide an additional way to modulate excitatory transmission and the induction of plasticity at excitatory synapses Thanks to recent technological advances progress has been made in understanding synaptic transmission and plasticity

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