Brain Structure and Function

, Volume 223, Issue 3, pp 1229–1253 | Cite as

Functional comparison of corticostriatal and thalamostriatal postsynaptic responses in striatal neurons of the mouse

  • M. A. Arias-García
  • D. Tapia
  • J. A. Laville
  • V. M. Calderón
  • Y. Ramiro-Cortés
  • J. Bargas
  • E. Galarraga
Original Article

Abstract

Synaptic inputs from cortex and thalamus were compared in electrophysiologically defined striatal cell classes: direct and indirect pathways’ striatal projection neurons (dSPNs and iSPNs), fast-spiking interneurons (FS), cholinergic interneurons (ChINs), and low-threshold spiking-like (LTS-like) interneurons. Our purpose was to observe whether stimulus from cortex or thalamus had equivalent synaptic strength to evoke prolonged suprathreshold synaptic responses in these neuron classes. Subthreshold responses showed that inputs from either source functionally mix up in their dendrites at similar electrotonic distances from their somata. Passive and active properties of striatal neuron classes were consistent with the previous studies. Cre-dependent adeno-associated viruses containing Td-Tomato or eYFP fluorescent proteins were used to identify target cells. Transfections with ChR2-eYFP driven by the promoters CamKII or EF1.DIO in intralaminar thalamic nuclei using Vglut-2-Cre mice, or CAMKII in the motor cortex were used to stimulate cortical or thalamic afferents optogenetically. Both field stimuli in the cortex or photostimulation of ChR2-YFP cortical fibers evoked similar prolonged suprathreshold responses in SPNs. Photostimulation of ChR2-YFP thalamic afferents also evoked suprathreshold responses. Differences previously described between responses of dSPNs and iSPNs were observed in both cases. Prolonged suprathreshold responses could also be evoked from both sources onto all other neuron classes studied. However, to evoke thalamostriatal suprathreshold responses, afferents from more than one thalamic nucleus had to be stimulated. In conclusion, both thalamus and cortex are capable to generate suprathreshold responses converging on diverse striatal cell classes. Postsynaptic properties appear to shape these responses.

Keywords

Striatum Striatal projection neurons Striatal interneurons Synaptic integration Intrinsic properties Corticostriatal pathway Thalamostriatal pathway 

Notes

Acknowledgements

We thank Gabriela X Ayala and Ariadna Aparicio for technical support and advice and Dr. Claudia Rivera for animal care. We thank Dr. Rene Druker-Colín for his help with transgenic animals. This work was supported by Consejo Nacional de Ciencia y Tecnología (México) Grant Frontera 57 to JB and 251144 to EG, and by Grants from Dirección General de Asuntos del Personal Académico. Universidad Nacional Autónoma de México: IN201417 and IN201517 to JB and EG. Mario A. Arias-García had a DGAPA and CONACyT doctoral fellowships and data in this work are part of his doctoral dissertation in the Doctorado en Ciencias Biomédicas de la Universidad Nacional Autónoma de México.

References

  1. Arias-García MA, Tapia D, Flores-Barrera E, Pérez-Ortega JE, Bargas J, Galarraga E (2013) Duration differences of corticostriatal responses in striatal projection neurons depend on calcium activated potassium currents. Front Syst Neurosci 7:63. doi: 10.3389/fnsys.2013.00063 PubMedPubMedCentralCrossRefGoogle Scholar
  2. Assous M, Kaminer J, Shah F, Garg A, Koós T, Tepper JM (2017) Differential processing of thalamic information via distinct striatal interneuron circuits. Nat Commun 8:15860. doi: 10.1038/ncomms15860 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Bargas J, Galarraga E, Aceves J (1991) Dendritic activity on neostriatal neurons as inferred from somatic intracellular recordings. Brain Res 539:159–163. doi: 10.1016/0006-8993(91)90700-6 PubMedCrossRefGoogle Scholar
  4. Beatty JA, Sullivan MA, Morikawa H, Wilson CJ (2012) Complex autonomous firing patterns of striatal low-threshold spike interneurons. J Neurophysiol 108:771–781. doi: 10.1152/jn.00283.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  5. Beatty JA, Song SC, Wilson CJ (2015) Cell-type-specific resonances shape the responses of striatal neurons to synaptic input. J Neurophysiol 113:688–700. doi: 10.1152/jn.00827.2014 PubMedCrossRefGoogle Scholar
  6. Bennett BD, Wilson CJ (1999) Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19:5586–5596PubMedGoogle Scholar
  7. Berendse HW, Groenewegen HJ (1990) Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J Comp Neurol 299:187–188. doi: 10.1002/cne.902990206 PubMedCrossRefGoogle Scholar
  8. Bonsi P, Cuomo D, Martella G, Madeo G, Schirinzi T, Puglisi F, Ponterio G, Pisani A (2011) Centrality of striatal cholinergic transmission in Basal Ganglia function. Front Neuroanat 5:6. doi: 10.3389/fnana.2011.00006 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Calabresi P, Centonze D, Gubellini P, Pisani A, Bernardi G (2000) Acetylcholine-mediated modulation of striatal function. Trends Neurosci 23:120–126. doi: 10.1016/S0166-2236(99)01501-5 PubMedCrossRefGoogle Scholar
  10. Carrillo-Reid L, Tecuapetla F, Tapia D, Hernández-Cruz A, Galarraga E, Drucker-Colin R, Bargas J (2008) Encoding network states by striatal cell assemblies. J Neurophysiol 99:1435–1450. doi: 10.1152/jn.01131.2007 PubMedCrossRefGoogle Scholar
  11. Carter AG, Sabatini BL (2004) State-dependent calcium signaling in dendritic spines of striatal medium spiny neurons. Neuron 44:483–493. doi: 10.1016/j.neuron.2004.10.013 PubMedCrossRefGoogle Scholar
  12. Castle M, Aymerich MS, Sanchez-Escobar C, Gonzalo N, Obeso JA, Lanciego JL (2005) Thalamic innervation of the direct and indirect basal ganglia pathways in the rat: ipsi- and contralateral projections. J Comp Neurol 483:143–153. doi: 10.1002/cne.20421 PubMedCrossRefGoogle Scholar
  13. Cowan RL, Wilson CJ (1994) Spontaneous firing patterns and axonal projections of single corticostriatal neurons in the rat medial agranular cortex. J Neurophysiol 71:17–32PubMedCrossRefGoogle Scholar
  14. Day M, Wokosin D, Plotkin JL, TianX Surmeier DJ (2008) Differential excitability and modulation of striatal medium spiny neuron dendrites. J Neurosci 28:11603–11614. doi: 10.1523/JNEUROSCI.1840-08.2008 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Dehorter N, Guigoni C, Lopez C, Hirsch J, Eusebio A, Ben-Ari Y, Hammond C (2009) Dopamine-deprived striatal GABAergic interneurons burst and generate repetitive gigantic IPSCs in medium spiny neurons. J Neurosci 29:7776–7787. doi: 10.1523/jneurosci.1527-09.2009 PubMedCrossRefGoogle Scholar
  16. Deng YP, Reiner A (2016) Cholinergic interneurons in the Q140 knockin mouse model of Huntington’s disease: reductions in dendritic branching and thalamostriatal input. J Comp Neurol 524:3518–3529. doi: 10.1002/cne.24013 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Deschênes M, Bourassa J, Parent A (1996a) Striatal and cortical projections of single neurons from the central lateral thalamic nucleus in the rat. Neuroscience 72:679–687. doi: 10.1016/0306-4522(96)00001-2 PubMedCrossRefGoogle Scholar
  18. Deschênes M, Bourassa J, Doan VD, Parent A (1996b) A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur J Neurosci 8:329–343. doi: 10.1111/j.1460-9568.1996.tb01217.x PubMedCrossRefGoogle Scholar
  19. Ding J, Peterson JD, Surmeier DJ (2008) Corticostriatal and thalamostriatal synapses have distinctive properties. J Neuroscience 28:6483–6492. doi: 10.1523/JNEUROSCI.0435-08.2008 CrossRefGoogle Scholar
  20. Ding JB, Guzman JN, Peterson JD, Goldberg JA, Surmeier DJ (2010) Thalamic gating of corticostriatal signaling by cholinergic interneurons. Neuron 67:294–307. doi: 10.1016/j.neuron.2010.06.017 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Doig NM, Moss J, Bolam JP (2010) Cortical and thalamic innervation of direct and indirect pathway medium-sized spiny neurons in mouse striatum. J Neurosci 30:14610–14618. doi: 10.1523/JNEUROSCI.1623-10.2010 PubMedCrossRefGoogle Scholar
  22. Doig NM, Magill PJ, Apicella P, Bolam JP, Sharott A (2014) Cortical and thalamic excitation mediate the multiphasic responses of striatal cholinergic Interneurons to motivationally salient stimuli. J Neurosci 34:3101–3117. doi: 10.1523/JNEUROSCI.4627-13.2014 PubMedPubMedCentralCrossRefGoogle Scholar
  23. Dube L, Smith AD, Bolam JP (1988) Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol 267:455–471. doi: 10.1002/cne.902670402 PubMedCrossRefGoogle Scholar
  24. Elghaba R, Vautrelle N, Bracci E (2016) Mutual control of cholinergic and low-threshold spike interneurons in the striatum. Front Cell Neurosci 10:111. doi: 10.3389/fncel.2016.00111 PubMedPubMedCentralCrossRefGoogle Scholar
  25. Ellender TJ, Harwood J, Kosillo P, Capogna M, Bolam JP (2013) Heterogeneous properties of central lateral and parafascicular thalamic synapses in the striatum. J Physiol 591:257–272. doi: 10.1113/jphysiol.2012.24 PubMedCrossRefGoogle Scholar
  26. English DF, Ibanez-Sandoval O, Stark E, Tecuapetla F, Buzsaki G, Deisseroth K, Tepper JM, Koos T (2011) GABAergic circuits mediate the reinforcement-related signals of striatal cholinergic interneurons. Nat Neurosci 15:123–130. doi: 10.1038/nn.2984 PubMedPubMedCentralCrossRefGoogle Scholar
  27. Faust TW, Assous M, Shah F, Tepper JM, Koós T (2015) Novel fast adapting interneurons mediate cholinergic-induced fast GABAA inhibitory postsynaptic currents in striatal spiny neurons. Eur J Neurosci 42:1764–1774. doi: 10.1111/ejn.12915 PubMedPubMedCentralCrossRefGoogle Scholar
  28. Faust TW, Assous M, Tepper JM, Koós T (2016) Neostriatal GABAergic interneurons mediate cholinergic inhibition of spiny projection neurons. J Neurosci 36:9505–9511. doi: 10.1523/JNEUROSCI.0466-16.2016 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Fieblinger T, Graves SM, Sebel LE, Alcacer C, Plotkin JL, Gertler TS, Chan CS, Heiman M, Greengard P, Cenci MA, Surmeier DJ (2014) Cell type-specific plasticity of striatal projection neurons in parkinsonism and l-DOPA-induced dyskinesia. Nat Commun 5:5316. doi: 10.1038/ncomms6316 PubMedPubMedCentralCrossRefGoogle Scholar
  30. Flores-Barrera E, Laville A, Plata V, Tapia D, Bargas J, Galarraga E (2009) Inhibitory contribution to suprathreshold corticostriatal responses: an experimental and modeling study. Cell Mol Neurobiol 29:719–731. doi: 10.1007/s10571-009-9394-2 PubMedCrossRefGoogle Scholar
  31. Flores-Barrera E, Vizcarra-Chacón BJ, Tapia D, Bargas J, Galarraga E (2010) Different corticostriatal integration in spiny projection neurons from direct and indirect pathways. Front Syst Neurosci 4:15. doi: 10.3389/fnsys.2010.00015 PubMedPubMedCentralGoogle Scholar
  32. Flores-Barrera E, Vizcarra-Chacón BJ, Bargas J, Tapia D, Galarraga E (2011) Dopaminergic modulation of corticostriatal responses in medium spiny projection neurons from direct and indirect pathways. Front Syst Neurosci 5:15. doi: 10.3389/fnsys.2011.00015 PubMedPubMedCentralCrossRefGoogle Scholar
  33. Fujiyama F, Unzai T, Nakamura K, Nomura S, Kaneko T (2006) Difference in organization of corticostriatal and thalamostriatal synapses between patch and matrix compartments of rat neostriatum. Eur J Neurosci 24:2813–2824PubMedCrossRefGoogle Scholar
  34. Galvan A, Smith Y (2011) The primate thalamostriatal systems: anatomical organization, functional roles and possible involvement in Parkinson’s disease. Basal Ganglia 1:179–189. doi: 10.1016/j.baga.2011.09.001 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Giménez-Amaya JM, McFarland NR, de las Heras S, Haber SN (1995) Organization of thalamic projections to the ventral striatum in the primate. J Comp Neurol 354:127–149. doi: 10.1002/cne.903540109 PubMedCrossRefGoogle Scholar
  36. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC (2010) Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J Neurosci 30:2223–2234. doi: 10.1523/JNEUROSCI.4870-09.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  37. Gittis AH, Hang GB, LaDow ES, Shoenfeld LR, Atallah BV, Finkbeiner S, Kreitzer AC (2011) Rapid target-specific remodeling of fast-spiking inhibitory circuits after loss of dopamine. Neuron 71:858–868. doi: 10.1016/j.neuron.2011.06.035 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Higley MJ, Sabatini BL (2010) Competitive regulation of synaptic Ca2+ influx by D2 dopamine and A2A adenosine receptors. Nat Neurosci 13:958–966. doi: 10.1038/nn.2592 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Huerta-Ocampo I, Mena-Segovia J, Bolam JP (2014) Convergence of cortical and thalamic input to direct and indirect pathway medium spiny neurons in the striatum. Brain Struct Funct 219:1787–1800. doi: 10.1007/s00429-013-0601-z PubMedCrossRefGoogle Scholar
  40. Hunnicutt BJ, Jongbloets BC, Birdsong WT, Gertz KJ, Zhong H, Mao T (2016) A comprehensive excitatory input map of the striatum reveals novel functional organization. Elife 28:5. doi: 10.7554/eLife.19103 Google Scholar
  41. Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koos T, Tepper JM (2010) Electrophysiological and morphological characteristics and synaptic connectivity of tyrosine hydroxylase-expressing neurons in adult mouse striatum. J Neurosci 30:6999–7016. doi: 10.1523/JNEUROSCI.5996-09.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  42. Ibanez-Sandoval O, Tecuapetla F, Unal B, Shah F, Koós T, Tepper JM (2011) A novel functionally distinct subtype of striatal neuropeptide Y interneuron. J Neurosci 31:16757–16769. doi: 10.1523/JNEUROSCI.2628-11.2011 PubMedPubMedCentralCrossRefGoogle Scholar
  43. Iwai H, Kuramoto E, Yamanaka A, Sonomura T, Uemura M, Goto T (2015) Ascending parabrachio-thalamo-striatal pathways: potential circuits for integration of gustatory and oral motor functions. Neuroscience 294:1–13. doi: 10.1016/j.neuroscience.2015.02.045 PubMedCrossRefGoogle Scholar
  44. Jahnsen H, Llinás R (1984) Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J Physiol 349:227–247PubMedPubMedCentralCrossRefGoogle Scholar
  45. Jáidar O, Carrillo-Reid L, Hernández A, Drucker-Colín R, Bargas J, Hernández-Cruz A (2010) Dynamics of the parkinsonian striatal microcircuit : entrainment into a dominant network state. J Neurosci 30:11326–11336. doi: 10.1523/JNEUROSCI.1380-10.2010 PubMedCrossRefGoogle Scholar
  46. Kawaguchi Y (1993) Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13:4908–4923PubMedGoogle Scholar
  47. Kawaguchi Y, Wilson CJ, Augood SJ, Emson PC (1995) Striatal interneurons: chemical, physiological and morphological characterization. Trends Neurosci 18:527–535. doi: 10.1016/0166-2236(95)98374-8 PubMedCrossRefGoogle Scholar
  48. Kita H (1993) GABAergic circuits of the striatum. Prog Brain Res 99:51–72PubMedCrossRefGoogle Scholar
  49. Kita H (1996) Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience 70:925–940. doi: 10.1016/0306-4522(95)00410-6 PubMedCrossRefGoogle Scholar
  50. Kocsis JD, Sugimori M, Kitai ST (1977) Convergence of excitatory synaptic inputs to caudate spiny neurons. Brain Res 124:403–413. doi: 10.1016/0006-8993(77)90942-8 PubMedCrossRefGoogle Scholar
  51. Koos T, Tepper JM (1999) Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat Neurosci 2:467–472. doi: 10.1038/8138 PubMedCrossRefGoogle Scholar
  52. Koos T, Tepper JM, Wilson CJ (2004) Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J Neurosci 24:7916–7922. doi: 10.1523/JNEUROSCI.2163-04.2004 PubMedCrossRefGoogle Scholar
  53. Kosillo P, Zhang YF, Threlfell S, Cragg SJ (2016) Cortical control of striatal dopamine transmission via striatal cholinergic interneurons. Cereb Cortex 26:4160–4169. doi: 10.1093/cercor/bhw252 PubMedCentralCrossRefGoogle Scholar
  54. Kreitzer AC, Malenka RC (2008) Striatal plasticity and basal ganglia circuit function. Neuron 60:543–554. doi: 10.1016/j.neuron.2008.11.005 PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lacey CJ, Bolam JP, Magill PJ (2007) Novel and distinct operational principles of intralaminar thalamic neurons and their striatal projections. J Neurosci 27:4374–4384. doi: 10.1523/JNEUROSCI.5519-06.2007 PubMedCrossRefGoogle Scholar
  56. Lambe EK, Aghajanian GK (2007) Prefrontal cortical network activity: opposite effects of psychodelic hallucinogens and D1/D5 dopamine receptor activation. Neuroscience 145:900–910PubMedPubMedCentralCrossRefGoogle Scholar
  57. Macchi G, Bentivoglio M, Molinari M, Minciacchi D (1984) The thalamo-caudate versus thalamo-cortical projections as studied in the cat with fluorescent retrograde double labeling. Exp Brain Res 54:225–239PubMedCrossRefGoogle Scholar
  58. Malliani A, Purpura DP (1967) Patterns of synaptic activities in lenticular and entopeduncular neurons. Brain Res 6:341–354PubMedCrossRefGoogle Scholar
  59. Marco LA, Copack P, Edelson AM (1973) Intrinsic connections of caudate neurons. Locally evoked intracellular responses. Exp Neurol 40:683–698PubMedCrossRefGoogle Scholar
  60. Matsumoto N, Minamimoto T, Graybiel AM, Kimura M (2001) Neurons in the thalamic CM–Pf complex supply striatal neurons with information about behaviorally significant sensory events. J Neurophysiol 85:960–976PubMedCrossRefGoogle Scholar
  61. Maurice N, Liberge M, Jaouen F, Ztaou S, Hanini M, Camon J, Deisseroth K, Amalric M, Kerkerian-Le Goff L, Beurrier C (2015) Striatal cholinergic interneurons control motor behavior and basal ganglia function in experimental parkinsonism. Cell Rep 13:657–666. doi: 10.1016/j.celrep.2015.09.034 PubMedCrossRefGoogle Scholar
  62. Minamimoto T, Kimura M (2002) Participation of the thalamic CM–Pf complex in attentional orienting. J Neurophysiol 87(6):3090–3101 doi: 10.1152/jn.00564.2001 PubMedCrossRefGoogle Scholar
  63. Minamimoto T, Hori Y, Kimura M (2005) Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308:1798–1801PubMedCrossRefGoogle Scholar
  64. Muñoz-Manchado AB, Foldi C, Szydlowski S, Sjulson L, Farries M, Wilson C, Silberberg G, Hjerling-Leffler J (2016) Novel striatal GABAergic interneuron populations labeled in the 5HT3a (EGFP) mouse. Cereb Cortex 26:96–105. doi: 10.1093/cercor/bhu179 PubMedCrossRefGoogle Scholar
  65. Munson JB, Sypert GW (1979) Properties of single fibre excitatory post-synaptic potentials in triceps surae motoneurones. J Physiol 296:329–342PubMedPubMedCentralCrossRefGoogle Scholar
  66. Parker PR, Lalive AL, Kreitzer AC (2016) Pathway-specific remodeling of thalamostriatal synapses in parkinsonian mice. Neuron 89:734–740. doi: 10.1016/j.neuron.2015.12.038 PubMedPubMedCentralCrossRefGoogle Scholar
  67. Partridge JG, Janssen MJ, Chou DY, Abe K, Zukowska Z, Vicini S (2009) Excitatory and inhibitory synapses in neuropeptide Y—expressing striatal interneurons. J Neurophysiol 102:3038–3045. doi: 10.1152/jn.00272 PubMedPubMedCentralCrossRefGoogle Scholar
  68. Pérez-Ortega J, Duhne M, Lara-Gonzalez E, Plata V, Gasca D, Galarraga E, Hernández-Cruz A, Bargas J (2016) Pathophysiological signatures of functional connectomics in parkinsonian and dyskinetic striatal microcircuits. Neurobiol Dis 91:347–361. doi: 10.1016/j.nbd.2016.02.023 PubMedCrossRefGoogle Scholar
  69. Pérez-Ramírez MB, Laville A, Tapia D, Duhne M, Lara-González E, Bargas J, Galarraga E (2015) KV7 channels regulate firing during synaptic integration in GABAergic striatal neurons. Neural Plast 2015:472676. doi: 10.1155/2015/472676 PubMedPubMedCentralCrossRefGoogle Scholar
  70. Perk CG, Wickens JR, Hyland BI (2015) Differing properties of putative fast-spiking interneurons in the striatum of two rat strains. Neuroscience 294:215–226. doi: 10.1016/j.neuroscience.2015.02.051 PubMedCrossRefGoogle Scholar
  71. Planert H, Szydlowski SN, Hjorth JJ, Grillner S, Silberberg G (2010) Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J Neurosci 30:3499–3507. doi: 10.1523/JNEUROSCI.5139-09.2010 PubMedCrossRefGoogle Scholar
  72. Plotkin JL, Surmeier DJ (2015) Corticostriatal synaptic adaptations in Huntington’s disease. Curr Opin Neurobiol 33:53–62. doi: 10.1016/j.conb.2015.01.020 PubMedPubMedCentralCrossRefGoogle Scholar
  73. Plotkin JL, Day M, Surmeier DJ (2011) Synaptically driven state transitions in distal dendrites of striatal spiny neurons. Nat Neurosci 14:881–888. doi: 10.1038/nn.2848 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Purpura DP, Malliani A (1967) I. Synaptic potentials and discharge characteristics of caudate neurons activated by thalamic stimulation. Brain Res 6:325–340PubMedCrossRefGoogle Scholar
  75. Raju DV, Shah DJ, Wright TM, Hall RA, Smith Y (2006) Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J Comp Neurol 499:231–243. doi: 10.1002/cne.21099 PubMedPubMedCentralCrossRefGoogle Scholar
  76. Rall W (1967) Distinguishing theoretical synaptic potentials computed for different soma-dendritic distributions of synaptic input. J Neurophysiol 30:1138–1168PubMedCrossRefGoogle Scholar
  77. Rall W, Burke RE, Holmes WR, Jack JJB, Redman SJ, Segev I (1992) Matching dendritic neuron models to experimental data. Physiol Rev 72:159–186CrossRefGoogle Scholar
  78. Ramanathan S, Hanley JJ, Deniau JM, Bolam JP (2002) Synaptic convergence of motor and somatosensory cortical afferents onto GABAergic interneurons in the rat striatum. J Neurosci 22:8158–8169PubMedGoogle Scholar
  79. Reyes A, Galarraga E, Flores-Hernández J, Tapia D, Bargas J (1998) Passive properties of neostriatal neurons during potassium conductance blockade. Exp Brain Res 120:70–84PubMedCrossRefGoogle Scholar
  80. Rudkin TM, Sadikot AF (1999) Thalamic input to parvalbumin-immunoreactive GABAergic interneurons. Organization in normal striatum and effect of neonatal decortication. Neuroscience 88:1165–1175. doi: 10.1016/S0306-4522(98)00265-6 PubMedCrossRefGoogle Scholar
  81. Saunders A, Huang KW, Sabatini BL (2016) Globus pallidus externus neurons expressing parvalbumin interconnect the subthalamic nucleus and striatal interneurons. PLoS One 11(2):e0149798. doi: 10.1371/journal.pone.0149798 PubMedPubMedCentralCrossRefGoogle Scholar
  82. Schlösser B, ten Bruggencate G, Sutor B (1999) Local disinhibition of neocortical neuronal circuits causes augmentation of glutamatergic and GABAergic synaptic transmission in the rat neostriatum in vitro. Exp Neurol 157:180–193PubMedCrossRefGoogle Scholar
  83. Sciamanna G, Tassone A, Mandolesi G, Puglisi F, Ponterio G, Martella G, Madeo G, Bernardi G, Standaert DG, Bonsi P, Pisani C (2012) Cholinergic dysfunction alters synaptic integration between thalamostriatal and corticostriatal inputs in DYT1 dystonia. J Neurosci 32:11991–12004. doi: 10.1523/JNEUROSCI.0041-12.2012 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Sciamanna G, Ponterio G, Mandolesi G, Bonsi P, Pisani A (2015) Optogenetic stimulation reveals distinct modulatory properties of thalamostriatal vs corticostriatal glutamatergic inputs to fast spiking interneurons. Sci Rep 5:16742. doi: 10.1038/srep16742 PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sidibé M, Smith Y (1999) Thalamic inputs to striatal interneurons in monkeys: synaptic organization and co-localization of calcium binding proteins. Neuroscience 89:1189–1208. doi: 10.1016/S0306-4522(98)00367-4 PubMedCrossRefGoogle Scholar
  86. Silberberg G, Bolam JP (2015) Local and afferent synaptic pathways in the striatal microcircuitry. Curr Opin Neurobiol 33:182–187. doi: 10.1016/j.conb.2015.05.002 PubMedCrossRefGoogle Scholar
  87. Smeal RM, Gaspar RC, Keefe KA, Wilcox KS (2007) A rat brain slice preparation for characterizing both thalamostriatal and corticostriatal afferents. J Neurosci Meth 159:224–235. doi: 10.1016/j.jneumeth.2006.07.007 CrossRefGoogle Scholar
  88. Smeal RM, Keefe KA, Wilcox KS (2008) Differences in excitatory transmission between thalamic and cortical afferents to single spiny efferent neurons of rat dorsal striatum. Eur J Neurosci 28:2041–2052. doi: 10.1111/j.1460-9568.2008.06505.x PubMedPubMedCentralCrossRefGoogle Scholar
  89. Smith Y, Raju DV, Pare JF, Sidibé M (2004) The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci 27:520–527. doi: 10.1016/j.tins.2004.07.004 PubMedCrossRefGoogle Scholar
  90. Smith Y, Raju D, Nanda B, Pare JF, Galvan A, Wichmann T (2009) The thalamostriatal systems anatomical and functional organization in normal and parkinsonian states. Brain Res Bull 78:60–68. doi: 10.1016/j.brainresbull.2008.08.015 PubMedCrossRefGoogle Scholar
  91. Stern EA, Kincaid AE, Wilson CJ (1997) Spontaneous subthreshold membrane potential fluctuations and action potential variability of rat corticostriatal and striatal neurons in vivo. J Neurophysiol 77(4):1697–1715 (PMID: 9114230) PubMedCrossRefGoogle Scholar
  92. Straub C, Saulnier JL, Bègue A, Feng DD, Huang KW, Sabatini BL (2016) Principles of synaptic organization of GABAergic interneurons in the striatum. Neuron 92:84–92. doi: 10.1016/j.neuron.2016.09.007 PubMedPubMedCentralCrossRefGoogle Scholar
  93. Surmeier DJ, Carrillo-Reid L, Bargas J (2011) Dopaminergic modulation of striatal neurons, circuits, and assemblies. Neuroscience 19:3–18. doi: 10.1016/j.neuroscience.2011.08.051 CrossRefGoogle Scholar
  94. Szydlowski SN, PollakDorocic I, Planert H, Carlén M, Meletis K, Silberberg G (2013) Target selectivity of feedforward inhibition by striatal fast-spiking interneurons. J Neurosci 33:1678–1683. doi: 10.1523/JNEUROSCI.3572-12.2013 PubMedCrossRefGoogle Scholar
  95. Tepper JM, Bolam JP (2004) Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14(6):685–692. doi: 10.1016/j.conb.2004.10.003 PubMedCrossRefGoogle Scholar
  96. Tepper JM, Wilson CJ, Koós T (2008) Feedforward and feedback inhibition in neostriatal GABAergic spiny neurons. Brain Res Rev 58:272–281. doi: 10.1016/j.brainresrev.2007.10.008 PubMedCrossRefGoogle Scholar
  97. Tepper JM, Tecuapetla F, Koós T, Ibáñez-Sandoval O (2010) Heterogeneity and diversity of striatal GABAergic interneurons. Front Neuroanat 4:150. doi: 10.3389/fnana.2010.00150 PubMedPubMedCentralCrossRefGoogle Scholar
  98. Thomas TM, Smith Y, Levey AI, Hersch SM (2000) Cortical inputs to m2-immunoreactive striatal interneurons in rat and monkey. Synapse 37:252–261. doi: 10.1002/1098-2396(20000915)37:4<252:AID-SYN2>3.0.CO;2-A PubMedCrossRefGoogle Scholar
  99. Tseng KY, Snyder-Keller A, O’Donnell P (2007) Dopaminergic modulation of striatal plateau depolarizations in corticostriatal organotypic cocultures. Psychopharmacology 191:627–640. doi: 10.1007/s00213-006-0439-7 PubMedCrossRefGoogle Scholar
  100. Ünal B, Shah F, Kothari J, Tepper JM (2015) Anatomical and electrophysiological changes in striatal TH interneurons after loss of the nigrostriatal dopaminergic pathway. Brain Struct Funct 220:331–349. doi: 10.1007/s00429-013-0658-8 PubMedCrossRefGoogle Scholar
  101. Vergara R, Rick C, Hernández- López S, Laville JA, Guzman JN, Galarraga E, Surmeier DJ, Bargas J (2003) Spontaneous voltage oscillations in striatal projection neurons in a rat cortico striatal slice. J Physiol 15:169–182. doi: 10.1113/jphysiol.2003.050799 CrossRefGoogle Scholar
  102. Vizcarra-Chacón B, Arias-García MA, Pérez-Ramirez MB, Flores-Barrera E, Tapia D, Drucker-Colin R, Bargas J, Galarraga E (2013) Contribution of different classes of glutamate receptors in the cortico-striatal polysynaptic responses from striatal direct and indirect projection neurons. BMC Neurosci 14:60. doi: 10.1186/1471-2202-14-60 PubMedPubMedCentralCrossRefGoogle Scholar
  103. Wall NR, De La Parra M, Callaway EM, Kreitzer AC (2013) Differential Innervation of direct and indirect-pathway striatal projection neurons. Neuron 79:347–360. doi: 10.1016/j.neuron.2013.05.014 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Wilson CJ (1986) Postsynaptic potentials evoked in spiny neostriatal projection neurons by stimulation of ipsilateral and contralateral neocortex. Brain Res 367:201–213. doi: 10.1016/0006-8993(86)91593-3 PubMedCrossRefGoogle Scholar
  105. Wilson CJ, Kawaguchi Y (1996) The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J Neurosci 16:2397–2410PubMedGoogle Scholar
  106. Wilson CJ, Chang HT, Kitai ST (1990) Firing patterns and synaptic potentials of identified giant aspiny interneurons in the rat neostriatum. J Neurosci 10:508–519PubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • M. A. Arias-García
    • 1
  • D. Tapia
    • 1
  • J. A. Laville
    • 1
  • V. M. Calderón
    • 1
  • Y. Ramiro-Cortés
    • 1
  • J. Bargas
    • 1
  • E. Galarraga
    • 1
  1. 1.División de Neurociencias, Instituto de Fisiología CelularUniversidad Nacional Autónoma de México (UNAM)Mexico CityMexico

Personalised recommendations