Contribution of different classes of glutamate receptors in the corticostriatal polysynaptic responses from striatal direct and indirect projection neurons

BMC Neuroscience

Elvira Galarraga¹  José Bargas¹  Rene Drucker-Colin¹  Dagoberto Tapia¹  Edén Flores-Barrera¹  Maria B Pérez-Ramírez¹  Mario A Arias-García¹  Bianca J Vizcarra-Chacón¹ 

[1] División de Neurociencias. Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México, DF, México

关键词: Corticostriatal inputs;    Striatum;    KAINATE;    AMPA;    NMDA;    Glutamate;    Synaptic integration;   

Others  :  1140256
DOI  :  10.1186/1471-2202-14-60

 received in 2013-02-07, accepted in 2013-06-07,  发布年份 2013

【 摘 要 】

Background

Previous work showed differences in the polysynaptic activation of GABAergic synapses during corticostriatal suprathreshold responses in direct and indirect striatal projection neurons (dSPNs and iSPNs). Here, we now show differences and similarities in the polysynaptic activation of cortical glutamatergic synapses on the same responses. Corticostriatal contacts have been extensively studied. However, several questions remain unanswered, e.g.: what are the differences and similarities in the responses to glutamate in dSPNs and iSPNs? Does glutamatergic synaptic activation exhibits a distribution of latencies over time in vitro? That would be a strong suggestion of polysynaptic cortical convergence. What is the role of kainate receptors in corticostriatal transmission? Current-clamp recordings were used to answer these questions. One hypothesis was: if prolonged synaptic activation distributed along time was present, then it would be mainly generated from the cortex, and not from the striatum.

Results

By isolating responses from AMPA-receptors out of the complex suprathreshold response of SPNs, it is shown that a single cortical stimulus induces early and late synaptic activation lasting hundreds of milliseconds. Prolonged responses depended on cortical stimulation because they could not be elicited using intrastriatal stimulation, even if GABAergic transmission was blocked. Thus, the results are not explained by differences in evoked inhibition. Moreover, inhibitory participation was larger after cortical than after intrastriatal stimulation. A strong activation of interneurons was obtained from the cortex, demonstrating that polysynaptic activation includes the striatum. Prolonged kainate (KA) receptor responses were also elicited from the cortex. Responses of dSPNs and iSPNs did not depend on the cortical area stimulated. In contrast to AMPA-receptors, responses from NMDA- and KA-receptors do not exhibit early and late responses, but generate slow responses that contribute to plateau depolarizations.

Conclusions

As it has been established in previous physiological studies in vivo, synaptic invasion over different latencies, spanning hundreds of milliseconds after a single stimulus strongly indicates convergent polysynaptic activation. Interconnected cortical neurons converging on the same SPNs may explain prolonged corticostriatal responses. Glutamate receptors participation in these responses is described as well as differences and similarities between dSPNs and iSPNs.

【 授权许可】

   
2013 Vizcarra-Chacón et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

Figure 5.

Figure 6.

Figure 7.

Figure 8.

【 参考文献 】

• [1]Chergui K, Bouron A, Normand E, Mulle C: Functional GluR6 Kainate receptors in the striatum: indirect downregulation of synaptic transmission. J Neurosci 2000, 20(6):2175-2182.
• [2]Dehorter N, Michel FJ, Marissal T, Rotrou Y, Matrot B, Lopez C, Humphries MD, Hammond C: Onset of pup locomotion coincides with loss of NR2C/D-mediated cortico-striatal EPSCs and dampening of striatal network immature activity. Front Cell Neurosci 2011, 5:24.
• [3]Jeun SH, Cho HS, Kim KJ, Li QZ, Sung KW: Electrophysiological characterization of AMPA and NMDA receptors in rat dorsal striatum. Korean J Physiol Pharmacol 2009, 13(3):209-214.
• [4]Logan SM, Partridge JG, Matta JA, Buonanno A, Vicini S: Long-lasting NMDA receptor-mediated EPSCs in mouse striatal medium spiny neurons. J Neurophysiol 2007, 98(5):2693-2704.
• [5]Stefani A, Chen Q, Flores-Hernandez J, Jiao Y, Reiner A, Surmeier DJ: Physiological and molecular properties of AMPA/Kainate receptors expressed by striatal medium spiny neurons. Dev Neurosci 1998, 20(2–3):242-252.
• [6]Kemp JM, Powell TP: The cortico-striate projection in the monkey. Brain 1970, 93(3):525-546.
• [7]Kita T, Kita H: The subthalamic nucleus is one of multiple innervations sites for long-range corticofugal axons: a single-axon tracing study in the rat. J Neurosci 2012, 32(17):5990-5999.
• [8]Hoffer ZS, Alloway KD: Organization of corticostriatal projections from the vibrissal representations in the primary motor and somatosensory cortical areas of rodents. J Comp Neurol 2001, 439(1):87-103.
• [9]Hoover JE, Hoffer ZS, Alloway KD: Projections from primary somatosensory cortex to the neostriatum: the role of somatotopic continuity in corticostriatal convergence. J Neurophysiol 2003, 89(3):1576-1587.
• [10]Pan WX, Mao T, Dudman JT: Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front Neuroanatomy 2010, 4:147.
• [11]Parent M, Parent A: Single-axon tracing study of corticostriatal projections arising from primary motor cortex in primates. J Comp Neurol 2006, 496(2):202-213.
• [12]Wilson CJ: Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex. Brain Res 1986, 367(1–2):201-213.
• [13]Bennett BD, Bolam JP: Synaptic input and output of parvalbumin- immunoreactive neurons in the neostriatum of the rat. Neurosci 1994, 62(3):707-719.
• [14]Calabresi P, Pisani A, Mercuri NB, Bernardi G: The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia. Trends Neurosci 1996, 19(1):19-24.
• [15]Cherubini E, Herrling PL, Lanfumey L, Stanzione P: Excitatory amino acids in synaptic excitation of rat striatal neurones in vitro. J Physiol 1988, 400:677-690.
• [16]English DF, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsáki G, Deisseroth K, Tepper JM, Koos T: GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nature Neurosci 2011, 15(1):123-130.
• [17]Gerfen CR, Young WS: Distribution of striatonigral and striatopallidal peptidergic neurons in both patch and matrix compartments: an in situ hybridization histochemistry and fluorescent retrograde tracing study. Brain Res 1988, 460(1):161-167.
• [18]Kita H: Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroci 1996, 70(4):925-940.
• [19]Kita H, Kosaka T, Heizmann CW: Parvalbumin-immunoreactive neurons in the rat neostriatum: a light and electron microscopic study. Brain Res 1990, 536(1–2):1-15.
• [20]Ramanathan S, Hanley JJ, Deniau JM, Bolam JP: Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 2002, 22(18):8158-8169.
• [21]Világi I, Kocsis P, Tarnawa I, Banczerowski-Pelyhe I: Effect of glutamate receptor antagonists on excitatory postsynaptic potentials in striatum. Brain Res Bull 1988, 46(6):483-486.
• [22]Wilson CJ, Chang HT, Kitai ST: Disfacilitation and long-lasting inhibition of neostriatal neurons in the rat. Exp Brain Res 1983, 51(2):227-235.
• [23]Cowan RL, Wilson CJ: Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 1994, 71(1):17-32.
• [24]Flores-Barrera E, Laville A, Plata V, Tapia D, Bargas J, Galarraga E: Inhibitory contribution to suprathreshold corticostriatal responses: An experimental and modeling study. Cell Mol Neurobiol 2009, 29(5):719-731.
• [25]Flores-Barrera E, Vizcarra-Chacon BJ, Tapia D, Bargas J, Galarraga E: Different corticostriatal integration in spiny projectionneurons from direct and indirect pathways. Front Syst Neurosci 2010, 4:15.
• [26]Tseng KY, Snyder-Keller A, O'Donnell P: Dopaminergic modulation of striatal plateau depolarizations in corticostriatal organotypic cocultures. Psychopharmacol 2007, 191(3):627-640.
• [27]Pang Z, Ling GY, Gajendiran M, Xu ZC: Enhanced excitatory synaptic transmission in spiny neurons of rat striatum after unilateral dopamine denervation. Neurosci Lett 2001, 308(3):201-205.
• [28]Kandel ER, Schwartz JH, Jessell TM: Principles of Neural Science. 4th edition. New York: McGraw-Hill; 2000.
• [29]Sandrini G, Serrao M, Rossi P, Romaniello A, Cruccu G, Willer JC: The lower limb flexion reflex in humans. Prog Neurobiol 2005, 77(6):353-395.
• [30]Molnár G, Oláh S, Komlósi G, Füle M, Szabadics J, Varga C, Barzó P, Tamás G: Complex events initiated by individual spikes in the human cerebral cortex. PLoS Biol 2008, 6(9):e222.
• [31]Ammari R, Lopez C, Bioulac B, Garcia L, Hammond C: Subthalamic nucleus evokes similar long lasting glutamatergic excitations in pallidal, entopeduncular and nigral neurons in the basal ganglia slice. Neurosci 2010, 166(3):808-818.
• [32]Lambe EK, Aghajanian GK: Prefrontal cortical network activity: opposite effects of psychedelic hallucinogens and D1/D5 dopamine receptor activation. Neurosci 2007, 145(3):900-910.
• [33]Vergara R, Rick C, Hernández-López S, Laville JA, Guzman JN, Galarraga E, Surmeier DJ, Bargas J: Spontaneous voltage oscillations in striatal projection neurons in a rat corticostriatal slice. J Physiol 2003, 553(Pt 1):69-182.
• [34]Stern EA, Kincaid AE, Wilson CJ: Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 1997, 77(4):1697-1715.
• [35]Carrilo-Reid L, Tecuapetla F, Tapia D, Hernández-Cruz A, Galarraga E, Drucker-Colin R, Bargas J: Encoding network states by striatal cell assemblies. J Neurophysiol 2008, 99(3):1435-1450.
• [36]Carrillo-Reid L, Tecuapetla F, Ibáñez-Sandoval O, Hernández-Cruz A, Galarraga E, Bargas J: Activation of the cholinergic system endows compositional properties to striatal cell assemblies. J Neurophysiol 2009, 101(2):737-749.
• [37]Carrillo-Reid L, Hernández-López S, Tapia D, Galarraga E, Bargas J: Dopaminergic modulation of the striatal microcircuit: receptor specific configuration of cell assemblies. J Neurosci 2011, 31(42):14972-14983.
• [38]Akopian G, Walsh JP: Corticostriatal paired-pulse potentiation produced by voltage-dependent activation of NMDA receptors and L-type Ca2+_ channels. J Neurophysiol 2002, 87(1):157-165.
• [39]Calabresi P, Centonze D, Pisani A, Sancesario G, Gubellini P, Marfia GA, Bernardi G: Striatal spiny neurons and cholinergic interneurons express differential ionotropic glutamatergic responses and vulnerability: implications for ischemia and Huntington's disease. Ann Neurol 1998, 43(5):586-597.
• [40]Carter AG, Soler-Llavina GJ, Sabatini BL: Timing and location of synaptic inputs determine modes of subthreshold integration in striatal medium spiny neurons. J Neurosci 2007, 27(33):8967-8977.
• [41]Cepeda C, Itri JN, Flores-Hernandez J, Hurst RS, Calvert CR, Levine MS: Differential sensitivity of medium- and large-sized striatal neurons to NMDA but not kainate receptor activation in the rat. Eur J Neurosci 2001, 14(10):1577-1589.
• [42]Gertler TS, Chan CS, Surmeier DJ: Dichotomous anatomical properties of adult striatal medium spiny neurons. J Neurosci 2008, 28(43):10814-10824.
• [43]Yin XT, Smith Y: Localization and functions of kainate receptors in the basal ganglia. In Kainate Receptors: Novel Signaling Insights. Volume 717. Edited by Rodríguez-Moreno A, Sihra TS. US: Springer; 2011:27-37.
• [44]Castillo PE, Malenka RC, Nicoll RA: Kainate receptors mediate a slow postsynaptic current in hippocampal CA3 neurons. Nature 1997, 388(6638):182-186.
• [45]West PJ, Dalpé-Charron A, Wilcox KS: Differential contribution of kainate receptors to excitatory postsynaptic currents in superficial layer neurons of the rat medial entorhinal cortex. Neurosci 2007, 146(3):1000-1012.
• [46]Contractor A, Mulle C, Swanson GT: Kainate receptors coming of age: milestones of two decades of research. Trends Neurosci 2011, 34(3):154-163.
• [47]Jane DE, Lodge D, Collingridge GL: Kainate receptors: pharmacology, function and therapeutic potential. Neuropharmacol 2009, 56(1):90-113.
• [48]Lerma J: Kainate receptor physiology. Curr Opin Pharmacol 2006, 6(1):89-97.
• [49]Ghasemzadeh MB, Sharma S, Surmeier DJ, Eberwine JH, Chesselet MF: Multiplicity of glutamate receptor subunits in single striatal neurons: an RNA amplification study. Mol Pharmacol 1996, 49(5):852-859.
• [50]Bischoff S, Barhanin J, Bettler B, Mulle C, Heinemann S: Spatial distribution of kainate receptor subunit mRNA in the mouse basal ganglia and ventral mesencephalon. J Comp Neurol 1997, 379(4):541-562.
• [51]Kieval JZ, Hubert GW, Charara A, Paré JF, Smith Y: Subcellular and subsynaptic localization of presynaptic and postsynaptic kainate receptor subunits in the monkey striatum. J Neurosci 2001, 21(22):8746-8757.
• [52]Cho JH, Bayazitov IT, Meloni EG, Myers KM, Carlezon WA Jr, Zakharenko SS, Bolshakov VY: Coactivation of thalamic and cortical pathways induces input timing-dependent plasticity in amygdala. Nat Neurosci 2011, 15(1):113-122.
• [53]Cui A, Mayer ML: Heteromeric kainate receptors formed by the coassembly of GluR5, GluR6, and GluR7. J Neurosci 1999, 19(19):8281-8291.
• [54]Perrais D, Pinheiro PS, Jane DE, Mulle C: Antagonism of recombinant and native GluR3-containing kainate receptors. Neuropharmacol 2009, 56(1):131-140.
• [55]Plotkin JL, Day M, Surmeier DJ: Synaptically driven state transitions in distal dendrites of striatal spiny neurons. Nat Neurosci 2011, 14(7):881-888.
• [56]Lerma J, Morales M, Vicente MA, Herreras O: Glutamate receptors of the kainate type and synaptic transmission. Trends Neurosci 1997, 20(1):9-12.
• [57]Mulle C, Sailer A, Swanson GT, Brana C, O’Gorman S, Bettler B, Heinemann SF: Subunit composition of kainate receptors in hippocampal interneurons. Neuron 2000, 28(2):475-484.
• [58]Schiller J, Schiller Y: NMDA receptor-mediated dendritic spikes and coincident signal amplification. Curr Opin Neurobiol 2001, 11(3):343-348.
• [59]Antic SD, Zhou WL, Moore AR, Short SM, Ikonomu KD: The decade of the dendritic NMDA spike. J Neurosci Res 2010, 88(14):2991-3001.
• [60]Surmeier DJ, Carrillo-Reid L, Bargas J: Dopaminergic modulation of striatal neurons, circuits, and assemblies. Neurosci 2011, 198:3-18.
• [61]Gruber AJ, O'Donnell P: Bursting activation of prefrontal cortex drives sustained up states in nucleus accumbens spiny neurons in vivo. Synapse 2009, 63(3):173-180.
• [62]Koós T, Tepper JM: Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 1999, 2(5):467-472.
• [63]Koós T, Tepper JM: Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 2002, 22(2):529-535.
• [64]Planert H, Szydlowski SN, Hjorth JJ, Grillner S, Silberberg G: Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J Neurosci 2010, 30(9):3499-3507.
• [65]Kawaguchi Y: Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 1993, 13(11):4908-4923.
• [66]Partridge JG, Janssen MJ, Chou DY, Abe K, Zukowska Z, Vicini S: Excitatory and inhibitory synapses in neuropeptide Y-expressing striatal interneurons. J Neurophysiol 2009, 102(5):3038-3045.
• [67]Deng P, Zhang Y, Xu ZC: Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons. J Neurosci 2007, 27(12):3148-3156.
• [68]Goldberg JA, Wilson CJ: Control of spontaneous firing patterns by the selective coupling of calcium currents to calcium-activated potassium currents in striatal cholinergic interneurons. J Neurosci 2005, 5(44):10230-10238.
• [69]Kawaguchi Y: Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J Neurophysiol 1992, 67(6):1669-1682.
• [70]Wilson CJ: The mechanism of intrinsic amplification of hyperpolarizations and spontaneous bursting in striatal cholinergic interneurons. Neuron 2005, 45(4):575-585.
• [71]Kreitzer AC, Malenka RC: Striatal plasticity and basal ganglia circuit function. Neuron 2008, 60(4):543-554.
• [72]Cossart R, Aronov D, Yuste R: Attractor dynamics of network UP states in the neocortex. Nature 2003, 423(6937):283-288.
• [73]Hahn G, Petermann T, Havenith MN, Yu S, Singer W, Plenz D, Nikolic´ D: Neuronal avalanches in spontaneous activity in vivo. J Neurophysiol 2010, 104(6):3312-3322.
• [74]Ikegaya Y, Aaron G, Cossart R, Aronov D, Lampl I, Ferster D, Yuste R: Synfire chains and cortical songs: temporal modules of cortical activity. Science 2004, 304(5670):559-564.
• [75]Plenz D, Thiagarajan TC: The organizing principles of neuronal avalanches: cell assemblies in the cortex? Trends Neurosci 2007, 30(3):101-110.
• [76]Wilson CJ, Chang HT, Kitai ST: Origins of post synaptic potentials evoked in spiny neostriatal projection neurons by thalamic stimulation in the rat. Exp Brain Res 1983, 51(2):217-226.
• [77]Wang W, Dever D, Lowe J, Storey GP, Bhansali A, Eck EK, Nitulescu I, Weimer J, Bamford NS: Regulation of prefrontal excitatory neurotransmission by dopamine in the nucleus accumbens core. J Physiol 2012, 590(16):3743-3769.