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  • Hippocampal Neurons and Plasticity

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    32 vues10 pages

    Hippocampal Neurons and Plasticity

    Transféré par

    wvickery_1
    neuroscience

    Droits d'auteur :

    Attribution Non-Commercial (BY-NC)
    Téléchargez comme PDF, TXT ou lisez en ligne sur Scribd
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    Neurpharmacogy 6 (2011 720-729 Contents lists available at ScienceDirect Neuropharmacology journal homepage: www.elsevier.com/locate/neuropharm ELSEVIER Invited review Induction and expression rules of synaptic plasticity in hippocampal interneurons Fernanda Laezza**, Raymond Dingledine” Univesity Teas Medal Branch, Deparment of Pharmacology Tcl 30! University Boulevard Galeton. X 7555, A nary Unversty Deparment of Prac Ala, GA USA ARTICLE INFO ABSTRACT ‘re aan Received 1 September 2010, ‘Accepted 15 Doerr 2010 ‘The mowledge that excitatory synapses on aspiny hippocampal interneurons can develop genie Trine of activty-dependent remodeling, independently ffom the surrounding network of principal cells, is 4 relatively new concept. Cumulative evidence has now unequivocally demonstrated that, despite the Shsence of spedalzed postsynaptic spines that serve as compartmentalized structure for intracellular Signaling in principal cell plasticity, excitatory inputs onto interneurons can undergo forms of synaptic plasticity that are induced and expressed autonomously from principal cells Yet, the rules for induction Saeeaans and expression of interneuron plasticity are much more heterogeneous than in principal neurons. Long- we term plasticity in interneurons is not necessarily dependent upon postsynaptic activation of NMDA eae ‘ecepfrs nor relies on the same postsynaptic membrane potential requirements 3s principal cell, las- Fatty tity in interneurons rather requires activation of Ca? -permeable AMPA receptors andjor metabotropie ippocns _slutamate receptors and is triggered by postsynaptic hyperpolrization. nthiseview we wil outline these distinct features of intemeuron plasticity and identify potential critical candidate molecules that might be important for sustaining long-lasting changes in synaptic strength at excitatory inputs onto interneurons “This article is part ofa Special Ise entitled Synaptic Plasticity & interneurons ‘2011 Elsevier Ld, Al rights reserved 1. Introduction a growing body of evidence indicates that interneurons are equipped with plastic synapses that adapt to activity (Kullmann That synaptic spines are specialized compartments critical for long-lasting activty-dependent remodeling in principal cells is ‘well known (Newpher and Ehlers, 2009), Postsynaptic spines in principal cells serve as an organized compartment for Ca** influx sensing and provide a structural substrate for the cell signaling machinery that sustains long-lasting synaptic plasticity. Interest- ingly, despite the fact that excitatory presynaptic terminals contact bot principal neurons and GABAergic interneurons, the micro anatomy of these two connections is strikingly different. Most ‘excitatory synapses on principal neurons are spiny, whereas most intemeuron dendrites are free of spines and receive excitatory inputs directly on shafts (Freund and Bu2saki, 1996). For years the absence of synaptic spines had been considered an argument ‘against the ability of interneurons to undergo synaptic plasticity independently from surrounding principal cells (MeBain et al 1999) Lacking visible postsynaptic microdomains, excitatory inputs on interneurons were believed to be deprived of the ‘molecular postsynaptic machinery needed for long-lasting synaptic Femodeling. This issue was disputed for a considerable time, but TT Coespending author Te: 1409772 9672: ae 1400 729682 ‘Eni adie elaczabutmibads(eLazzah (908-2008) — sce toot mutter 2071 Eker tA eights esr {So:101016, europa 201012016 and Lamsa, 2007; Pelletier and Lacaille, 2008). However, the rules Of induction and expression of plasticity appear different and possibly more heterogeneous for interneurons in comparison to principal neurons (Kullmann and Lamsa, 2008). Long-term plas- ticity in interneurons is not necessarily dependent upon post- synaptic activation of N-methyl-o-aspartic acid (NMDA) receptors nor relies on the same postsynaptic membrane potential require- ‘ments as principal cells and, even though spines ate infrequent, organized postsynaptic molecular domains exist in interneurons that can serve as compartmentalized structures for spatially restricted intracellular signaling. While revealing a fundamental difference between synaptic structures in interneurons versus principal cell, the lack of anatomical spines does not preclude interneurons developing genuine forms of synaptic plasticity. An ‘open challenge will be to determine the structure of pre and postsynaptic compartments at excitatory inputs on interneurons And unravel the functional rules for induction and expression of | ‘synaptic plasticity. The goals of this review are to: i) outline the forms of plasticity found in interneurons; i) identify pre and post- synaptic receptors and/or molecules that have been implicated in induction andjor expression of plasticity in interneurons: ii) introduce novel targets with potential roles in interneuron plasticity. Our hope is to create a template that might serve as taza, Dingle /Neopharmaclgy 60 (201) 720-723 m guidance and intellectual. stimulus for innovative scientific ‘Ventures in this growing field of neuroscience. 2. Mechanisms of induction of synaptic plasticity, in interneurons 21, AMPA receptor-dependent plasticity ‘One of the most striking diflerences between synaptic plasticity in hippocampal interneurons and pyramidal cells isthe differential roles f1-amino-3-bydroxy-5-methyl-4-isoxazole-propionate (AMPA) receptors inthe induction of synaptic remodeling. AMPA receptors are heterotetramers formed by the heterologous combination of GluA1-GluA4 subunits; these subunits determine ionic perme- ability and contribute tothe biophysical properties of the channel (Traynelis et al, 2010), AMPA receptors mediate fast excitatory ‘synaptic transmission in both principal cellsand interneurons. Once activated by presynaptic glutamate release, they elicit excitatory postsynaptic currents (EPSCs), which are notably different in the two cell populations. Typically, interneurons express a considerable lower level of the GIuA2 subunit compared to pyramidal cells (Geiger et a. 1995; Washburn et al, 1997). GluA2- Ol es aaee eto de Ha. x distance (um) —Control (¢-APV) —cx-546 ig. Two-phutn mages of Ca" tansents mediated by C-ANA recor in cori inert, (Aa) Aaa dedi wih the Ca dye oA) Tp. cota line sian tough deat fa}, average af ree Sucenses Vr sel 40 ms Bottom, AFF age ram ne San above Vera le, 10 ms (A) ages re presented 2518 (Ab afer addon o 1 M546 an nua of AMPA secepor deacon. Nate how the azodonain sed a ace deni Segment Avago fou sucess. (ta) versus dente space pl ar clr ease in (AD) (8) Data lated as nar the vase the presence of C545 Note tha als ih) {38 (Top. calclum uagstents rm backeted eins be Scns (A belt ackttae, anal ed aditn of 546. oto, ESC tine laced othe au tases ‘Shove: Note how X46 dant prolonged the AMPA ceptors currents Al the expetents were peranned inte presence of te NMBA ede Blocker AV (amines -posphanateric acd) Modied fom Clery el, Neato 203 ‘CaMJaCaMKil complex is not a requirement for interneuron plas- ticity: Possibly, CAMIL, an isoform that is more prominent in ‘some interneurons (Wang and Kelly, 2001), other kinases such as ‘CaMKI and CaMKIV (Soderling, 1999), might play redundant roles land compensate for the lack of functional CAMEL Notably, ‘emerging evidence indicates that Ca" binding proteins enriched in intereurons, such as calbindin, caltetinin and parvalbumin, in addition to operating as Ca"* bulers, might serve as Ca** sensors that provide an alternative Caé* route to CaM (Burgoyne et al, 2004) ‘Another possibility to consider is that CP-AMPA receptor plas- ticity might rely on a diferent class of kinases. For example, recent ‘evidence has revealed a novel form of LIP triggered by CP-AMPA in CAI pyramidal neurons that engages a PI3-kinase/MAPK cascade rather than 2CAMKI (Asrar tal, 2009) This pathway might be the default pathway linked to CP-AMPA receptors, at both interne and principal cells as an alternative to aCaMiKIL ‘More evidence is available for the role of PKA and PKC i erneuron plasticity. A form of NMDA receptor-independent LTP at mossy bers to CA3_lacunosum moleculare interneuron ‘synapses expressing CLAMPA requires postsynaptic activation of PKA (Calvan et al, 2010), similar to the LTP produced by these same inputs onto CA3_ pyramidal neurons (Dully and Nguyen, 2003; Huang and Kandel, 1994), However, extracellular applica- tion of a PKA inhibitor isnot sufficient to prevent a form of LTP at the synapse made by mossy fibers onto inhibitory basket cells i the dentate gyrus (Alle etal, 2001), indicating that PKA activa- tion isnot required for all forms of interneuron plasticity taza, Digi /Reopharmaclgy 60 (200) 720-723 ns Presynaptic activation of PKA is required for internalization of presynaptic mGlu7 in a form of LTP at mossy fibers to CA3 stratum lucidum interneurons (Pelkey et al, 2008) further sup- porting a role of this kinase in intemeuron plasticity, both pre ‘and postsynaptically. PKC activation in conjunction with PKA is required for LTP at mossy fbers to CA3 lacunosum moleculare intemeuron synapses (Galvan et al, 2010), PKC engagement has also been described in conjunction with dendritic Ca" signaling at inputs f0 CAL stratum alveus-oriens (Topolnik et al, 2009) and ‘during mGlu7-dependent LTD at the mossy fiber inputs to CA3 stratum lucidum intemeurons (Pelkey et al, 2005). Thus, although there are some likely similar signaling cascades under” lying expression of plasticity in interneurons and pyramidal cells, plasticity in interneurons does not exclusively depend upon ‘CaMKII activation as in principal cells, and none of the kinases that appear to mediate interneuron’ plasticity appears to be universally required for plasticity. One issue that should be addressed is whether the differences in Ca?*-induced kinase activity requirement are specif for interneurons or are dictated by phenotypic expression of postsynaptic receptors (for example, NMDA vs CP-AMPA receptors) 3.4. PDZ domain binding proteins and other postsynaptic molecules The role of scaffolding proteins in the expression of synaptic plasticity in interneurons is largely unknown and the repertoire of studies on the expression and distribution of these molecules in hippocampal interneurons is limited (Craig et al, 2006; Kim and Sheng, 2004; Penzes et al, 2000; Tomita et al. 2001). The PDZ domain is a common structural domain found in a number of proteins. Within the POZ domain family of proteins localized in synaptic spines, (Craig etal, 2006; Ma, 2010; Ma et al, 2010, 2008; Zhang et al, 1999), PSD-95 has been found enriched postsynaptically in hippocampal interneurons: its overexpression increased the numberof GIuAI clusters in dendeiti shafts and the frequency of miniature EPSCs (El-Husseini etal, 2000), suggesting . potential role of PSD-95 in stabilizing or inserting AMPA receptors in interneurons. Other PDZ domain proteins, such as the GRIP3/ b isoforms, are also expressed in interneurons, although at low levels (Charych et al. 2006, 2004); these could also be critical for AMPA receptor stability and traffcking in interneurons, but there are no available studies on this matte. Interestingly, in stellate inhibitory neurons ofthe cerebellum, the interaction of PICK and GluA2 controls mobility of AMPA receptors in a form of synaptic plasticity expressed as a switch in AMPA receptor composition, Consisting in increase of synaptic GluA2 content and decrease in AMPA receptor Ca** permeability (Liu and Cull-Candy, 2002, 2005, 2000). The same mechanism might underlie CP-AMPA receptor” ‘dependent plasticity in hippocampal interneurons and should be examined, 3.5. AMPA receptor trafficking There has been only one report of a potential involvement of AMPA receptor trafficking as a mechanism for expression of inter- neuron plasticity. Similar to reports in principal cells (Kessels and Malinow, 2009), a peptide inhibiting the activity of the AP2- clathtin adaptor protein 2 occludes LTD expression at mossy Fbers to CLAMPA receptor synapses but not at CP-AMPA receptor synapses of stratum lucidum interneurons, suggesting that acla- Utin-induced endocytosis of AMPA receptors might underlie the reduction in postsynaptic AMPA receptor trafficking (Lei and McBain, 2004) and serve as a mechanism of LTD expression, However, this mechanism appears to be specific for synapses expressing CI-AMPA receptors, and as such, more similar to exit- tory synapses in principal cell, GFP + HA-GluA2 ig. 2. Cut? intuces deni spins in GANA sling iaterneions Hippocampal neon at DIVA were asec with enhanced een orescentpot (EGFP) lone 0 ‘nthe same neon, as inated Icereurons (deind by typical dendsi morphology and GADS mmporeactvity in eso) have no dete spines when transfected with panels Show ghee magn atin fhe dene (CFP nage} Seale 10 ya ow mugaeaion) ahd 25 (high magneton a dr Pasa Ne 203. Principal cell4tike taza, Digi / Meopharmacly 60 (201) 720-723 Interneuro: ce ‘GluA2-rich synapses GIUA2-deficient synapses Da cH 70 CaMIKil, PKA, PKC PISKIMAPK toa receptors CP-s0NPA receptors JLsype ca chamels [J CLAMPA receptors ] rcureeqies PPylostoenesnte ig. 3. Working model iaternewon plastity. At tern saps coating: AMPA receptors (Clue) the mechanisms of induction and exes of synaptic sy might flow Hetan rues an be mae sino pcp el Camera nteneuronSyapses contin CAMA recep (CuA2 defen) the mechnss ‘tindction and expression of spt ply lows an Hebtan rus and ight equ ile nace signaling cascades 3.6. Structural plasticity Although structural plasticity in interneurons has not yet been ‘demonstrated, compelling evidence indicates that synaptic spines ‘can be induced in aspiny intemeurons upon overexpression of selected synaptic components, suggesting that the cytoskeleton of interneurons is dynamic and might therefore provide a structural basis for dynamic remodeling underlying synaptic plasticity. One of | the fist lines of evidence for spine- induction in interneurons came from Passafaro etal. (2003). In this milestone study, the authors reported that spines were induced on interneuron dendrite shafts by overexpression of the GIuA2 subunit (He et a, 1998; Passalaro et al, 2003) a illustrated in Fig. 2. In more recent studies, kalitin- 7, a multifunctional Rho GEF exchange protein that acts as a post- synaptic seaffold and co-localizes with PSD-95 at excitatory synapses onto interneuron dendritic shafts (Ma, 2010: Ma et a. 2010, 2008), has been shown to play similar roles. Whereas eduction of kalirin-7 levels reduces the size of PSD-95-positive puncta, overexpression of Kalirin-7 increases dendritic branching and induces the formation of spine-like structures along the ‘dendrites of aspiny hippocampal interneurons by a PDZ-mediated ‘mechanism (Ma, 2010; Ma et al, 2010, 2008). Collectively the role ‘of GIuA2 and of kalirin-7 demonstrates an important concept, ramely that spines can be induced in aspiny interneurons and that these aspiny shafts are dynamic molecular structures. Of obvious importance would be to determine whether upon synaptic remodeling, changes inthe level of GIuA2 expression converts CP- AMPA receptor aspiny synapses into GluA2 containing C-AMPA receptors and thus switches aspiny interneurons into spiny neurons. Furthermore, the composition of the cytoskeleton in ‘dendritic shafts or in induced synaptic spines in interneurons has not been studied yet Given the role of the Rho pathway in mediating structural plasticity in principal neurons, other molecules of the Rho family found in interneurons, such’ as Citron-N (citron) (Zhang and Benson, 2006), might also be considered as candidate substrates underlying structural remodeling of interneuron synapses. Furthermore, other cytoskeleton-associated molecules such as ‘z-actinin-2, a protein that provides a scaffolding bridge between NMDA receptors and membrane lipids (Michaiidis et al, 2007) hhave been identified in interneurons (Rataiff and Soltesz, 2001). Given that the interaction between 2-actinin-2 and NMDA tecep- {ors is regulated by CaM in principal neurons (Merrill et a, 2007), this molecule might also be a candidate for structural plasticity Collectively these results indicate that excitatory inputs onto interneurons are equipped with specific and unique combinations ff pre and postsynaptic glutamate receptor subtypes that confer distinctive means for differential decoding of high-frequency Inputs, resulting in enhanced or depressed transmission depending fn the Functional state of the interneuron. Compared to plasticity ‘mechanisms operating in principal neurons, interneuron plasticity {slifferent in the following waysas discussed above. Fist, although the dendritie structure of interneurons is dynamic and spines can be induced, aspiny synapses do not prevent signaling compart- ‘mentalization. Second, postsynaptic C2** entry during the induc- tion phase of plasticity in interneurons might be even faster than principal cells as dictated by the kinetics of CP-AMPA receptors Third, in contrast to principal cells, the postsynaptic signaling cascade that triggers interneuron plasticity does not necessarily involve CaMKl (at least for LTP); nor appear to present a universal requirement for any single kinase, although PKA and PKC have been found critical for some forms of interneuron plasticity. Fourth, CP- AMPA receptors play a much more prominent role inthe induction of synaptic plasticity in interneurons compared to principal cells. Although a universal scheme to describe the mechanisms of induction and expression of synaptic plasticity in interneurons is stil lacking, the level of GluA2 content in interneuron synapses appears to be the critical determinant of whether an interneuron synapse will phenotypically resemble principal cell synapses. Based fon the fragmentary and heterogeneous data on this topic, we propose a tentative working model in which we envision two extreme forms of interneuron plasticity based on the content of synaptic GluA2 (Fig. 3. In principal cell-like forms of plasticity, high levels of synaptic GluA2 might be typically associated with Hebbian forms of plasticity induced by activation of NMDA receptors (Lamsa et al, 2005; Maccaferri and MeBain, 1996; MeMahon and Kauer, 1997; Ouardouz and Lacaille, 1995), Ltype C32 channels (Calvan et al, 2008) andjor mGlu receptors (Galvan et al, 2008: taza, Dingle /Neopharmaclgy 60 (201) 720-723 m= ‘Ouardouz and Lacaille, 1995); this form of plasticity could depend ‘upon activation of CaMKAI (Wang and Kelly, 2001), PKA andor PKC (Calvan et al, 2008, 2010). Alternatively. synapses with low GluA2 synaptic content might be primarily but notexclusively (Le Vasseur cet al, 2008; Laezza and Dingledine, 2004), associated with anti- Hebbian, NMDA receptor-independent forms of plasticity that require postsynaptic hyperpolarization during induction (Laezza and Dingledine, 2004; Laezza et al, 1999; Lamsa et al, 2007b). ‘Whether this form of plasticity requires a PISK/MAPK-dependent intracellular signaling cascade (Astar et al, 2008), or is expressed through a PICKI-dependent trafficking of GluA2 containing AMPA receptors (Liu and Cull-Candy, 2002, 2005, 2000) that drives new spine formation (Passafaro et al, 2003), should be of immediate interest. Furthermore, identifying the physiological or pathophys- iological conditions that convert a GluA2-defiient into a CluA2- rich synapse, as part of an interneuron-like plastic remodeling, ‘would be another challenging and fascinating issue to address. Adknowledgements This work was supported by NINDS grant ROI NS36604 (RD) and bya grant from the institute for Translational Sciences at UTMB(FL). References ‘All, H Jos P, Geiger, JR 2001 PUP and LIP a a hippocampal assy Fer inzrheuon yrs. ho. NL Acad So USA, 1705-14713 Aww 2008, Hetaotopc glutamate receptor dependent lng en pte hon Newroparracloy 98 735-720. ‘Aart ou et W, a, 22009, Ca) permeable AMPA receptor induced Tg ee pe eis PMA esto CAC depen ts €- Gat Cot, 2007 The interaction beween Stags ae PSD-95 egultes AMPA receptor sure talfcing Neon 33, 719-734 ist Lv, Callngridge, GL. 1903. 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