Differential Excitability and Modulation of Striatal Medium Spiny Neuron Dendrites

Day, Michelle; Wokosin, David L.; Plotkin, Joshua L.; Tian, Xinyoung; Surmeier, D. James

doi:10.1523/jneurosci.1840-08.2008

Cited by 221 publications

(258 citation statements)

References 60 publications

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“…Recordings were performed on a submersion-style recording chamber with a fixed-stage Olympus BX51 upright microscope with continual perfusion of 95% O 2 /5% CO 2 bubbled artificial cerebrospinal fluid (in millimolar concentration): 124 NaCl, 3 KCl, 2 CaCl 2 , 1 MgCl 2 , 26 NaHCO 3 , 1 NaH 2 PO 4 , and 16.66 glucose with (in micromolar concentration) 100.0 4-AP, 1.0 TTX, 10.0 gabazine, and 1.0 CGP 35348. tdTomato expression was used to verify D1-MSNs. Whole-cell patch clamp recordings were made using a Multiclamp 700B amplifier using custom-written freeware package WinFluor (John Dempster, University of Strathclyde, Glasgow, UK) as described (62,71). Miniature excitatory postsynaptic currents (mEPSCs) were recorded in voltage clamp held at −70 mV.…”

Section: Methodsmentioning

confidence: 99%

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

Ceglia

Lee

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Wiskott-Aldrich syndrome protein (WASP) family verprolin homologous protein 1 (WAVE1) regulates actin-related protein 2/3 (Arp2/3) complex-mediated actin polymerization. Our previous studies have found WAVE1 to be inhibited by Cdk5-mediated phosphorylation in brain and to play a role in the regulation of dendritic spine morphology. Here we report that mice in which WAVE1 was knocked out (KO) in neurons expressing the D1 dopamine receptor (D1-KO), but not mice where WAVE1 was knocked out in neurons expressing the D2 dopamine receptor (D2-KO), exhibited a significant decrease in place preference associated with cocaine. In contrast to wild-type (WT) and WAVE1 D2-KO mice, cocaine-induced sensitized locomotor behavior was not maintained in WAVE1 D1-KO mice. After chronic cocaine administration and following withdrawal, an acute cocaine challenge induced WAVE1 activation in striatum, which was assessed by dephosphorylation. The cocaine-induced WAVE1 dephosphorylation was attenuated by coadministration of either a D1 dopamine receptor or NMDA glutamate receptor antagonist. Upon an acute challenge of cocaine following chronic cocaine exposure and withdrawal, we also observed in WT, but not in WAVE1 D1-KO mice, a decrease in dendritic spine density and a decrease in the frequency of excitatory postsynaptic AMPA receptor currents in medium spiny projection neurons expressing the D1 dopamine receptor (D1-MSNs) in the nucleus accumbens. These results suggest that WAVE1 is involved selectively in D1-MSNs in cocaine-evoked neuronal activitymediated feedback regulation of glutamatergic synapses.W iskott-Aldrich syndrome protein (WASP) family verprolin homologous protein (WAVE) initiates de novo actin polymerization through its ability to activate the actin-related protein 2/3 (Arp2/3) complex (1). Three members of the family (WAVE1-3) exist, with WAVE1 being highly expressed in brain (2). WAVE1 was purified from bovine or rat brain as part of a heteropentameric protein complex together with PIR121 [also called cytoplasmic FMR1-interacting protein 2, (Cyfip2)], Nck-associated protein 1 (Nckap1), Abl-interactor 2 (Abi2), and HSPC300 (3, 4). Whereas WAVE1 plays a key role in Arp2/3 complex binding and actin polymerization, other protein components in the complex are important for its subcellular localization and interaction with upstream ligands or activators (5, 6).In our initial study in striatum, the WAVE1 complex was found to interact with p35, the regulatory subunit of cyclin-dependent kinase 5 (Cdk5) (4). Phosphorylation of WAVE1 at Ser310, Ser397, and Ser441 by Cdk5/p35, in the complex purified from rat brain, or with recombinant WAVE1, resulted in inhibition of actin polymerization in vitro (4). We also observed that the stoichiometry of WAVE1 phosphorylation by Cdk5 is high in brain, suggestive of the protein being largely inactive under basal conditions (4). However, studies using mouse striatal slices indicated that WAVE1 can be dephosphorylated at all three Cdk5 sites and thereby activated upon stimulation of D1 dopa...

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Section: Methodsmentioning

confidence: 99%

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

Ceglia

Lee

Cahill

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…The development of BAC transgenic mice in which EGFP reports the expression of dopamine D 1 or D 2 receptors and hence direct or indirect pathway MSNs has been critical in the elucidation of the properties of these subpopulations of MSNs (Gong et al, 2003;Lobo et al, 2006;Kreitzer and Malenka, 2007;Surmeier et al, 2007;Ade et al, 2008;Cepeda et al, 2008;Day et al, 2008;Gertler et al, 2008;Shen et al, 2008;Shuen et al, 2008;Janssen et al, 2009). This development, together with the discovery that VGluT1 and VGluT2 selectively label corticostriatal and thalamostriatal afferents (Fremeau et al, 2004), enabled us to directly assess and quantify the relationship between excitatory afferents and the principal neurons of the striatum.…”

Section: Cortical and Thalamic Input To Direct And Indirect Pathway Msnsmentioning

confidence: 99%

Cortical and Thalamic Innervation of Direct and Indirect Pathway Medium-Sized Spiny Neurons in Mouse Striatum

Doig¹,

Moss²,

Bolam³

2010

J. Neurosci.

203

173

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The striatum receives major excitatory inputs from the cortex and thalamus that predominantly target the spines of medium-sized spiny neurons (MSNs). We aimed to determine whether there is any selectivity of these two excitatory afferents in their innervation of direct and indirect pathway MSNs. To address this, we used bacterial artificial chromosome transgenic mice, in which enhanced green fluorescent protein (EGFP) reports the presence of D 1 or D 2 dopamine receptor subtypes, markers of direct and indirect pathway MSNs, respectively. Excitatory afferents were identified by the selective expression of vesicular glutamate transporter type 1 (VGluT1) by corticostriatal afferents and vesicular glutamate transporter type 2 (VGluT2) by thalamostriatal afferents. A quantitative electron microscopic analysis was performed on striatal tissue from D 1 and D 2 mice that was double immunolabeled to reveal the EGFP and VGluT1 or VGluT2. We found that the proportion of synapses formed by terminals derived from the cortex and thalamus was similar for both direct and indirect pathway MSNs. Furthermore, qualitative analysis revealed that individual cortical or thalamic terminals form synapses with both direct and indirect pathway MSNs. Similarly, we observed a convergence of cortical and thalamic inputs onto individual MSNs of both direct and indirect pathway: individual EGFP-positive structures received input from both VGluT2-positive and VGluT2-negative terminals. These findings demonstrate that direct and indirect pathway MSNs are similarly innervated by cortical and thalamic afferents; both projections are thus likely to be critical in the control of MSNs and hence play fundamental roles in the expression of basal ganglia function.

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“…Kv4 channels in the spiny neurons of the striatal medium regulate b-AP (Day et al 2008) and participate in clustering and firing bursting patterns (Falk et al 2006). In addition, these channels play an essential role in producing an A-type current in striatal cholinergic interneurons (Hattori et al 2003).…”

Section: Spatial Learning Is Related To Transient Kv4 Up-regulationmentioning

confidence: 99%

Kv4 potassium channels modulate hippocampal EPSP-spike potentiation and spatial memory in rats

Truchet¹,

Manrique²,

Sréng³

et al. 2012

Learn. Mem.

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Kv4 channels regulate the backpropagation of action potentials (b-AP) and have been implicated in the modulation of longterm potentiation (LTP). Here we showed that blockade of Kv4 channels by the scorpion toxin AmmTX3 impaired reference memory in a radial maze task. In vivo, AmmTX3 intracerebroventricular (i.c.v.) infusion increased and stabilized the EPSP-spike (E-S) component of LTP in the dentate gyrus (DG), with no effect on basal transmission or short-term plasticity. This increase in E-S potentiation duration could result from the combination of an increase in excitability of DG granular cells with a reduction of GABAergic inhibition, leading to a strong reduction of input specificity. Radioactive in situ hybridization (ISH) was used to evaluate the amounts of Kv4.2 and Kv4.3 mRNA in brain structures at different stages of a spatial learning task in naive, pseudoconditioned, and conditioned rats. Significant differences in Kv4.2 and Kv4.3 mRNA levels were observed between conditioned and pseudoconditioned rats. Kv4.2 and Kv4.3 mRNA levels were transiently up-regulated in the striatum, nucleus accumbens, retrosplenial, and cingulate cortices during early stages of learning, suggesting an involvement in the switch from egocentric to allocentric strategies. Spatial learning performance was positively correlated with the levels of Kv4.2 and Kv4.3 mRNAs in several of these brain structures. Altogether our findings suggest that Kv4 channels could increase the signal-to-noise ratio during information acquisition, thereby allowing a better encoding of the memory trace.

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Differential Excitability and Modulation of Striatal Medium Spiny Neuron Dendrites

Cited by 221 publications

References 60 publications

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

WAVE1 in neurons expressing the D1 dopamine receptor regulates cellular and behavioral actions of cocaine

Cortical and Thalamic Innervation of Direct and Indirect Pathway Medium-Sized Spiny Neurons in Mouse Striatum

Kv4 potassium channels modulate hippocampal EPSP-spike potentiation and spatial memory in rats

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