Skip to main content
Log in

Roles of μ-Opioid Receptors in GABAergic Synaptic Transmission in the Striosome and Matrix Compartments of the Striatum

  • Published:
Molecular Neurobiology Aims and scope Submit manuscript

Abstract

The striatum is divided into two compartments, the striosomes and extrastriosomal matrix, which differ in several cytochemical markers, input–output connections, and time of neurogenesis. Since it is thought that limbic, reward-related information and executive aspects of behavioral information may be differentially processed in the striosomes and matrix, respectively, intercompartmental communication should be of critical importance to proper functioning of the basal ganglia-thalamocortical circuits. Cholinergic interneurons are in a suitable position for this communication since they are preferentially located in the striosome-matrix boundaries and are known to elicit a conditioned pause response during sensorimotor learning. Recently, μ-opioid receptor (MOR) activation was found to presynaptically suppress the amplitude of GABAergic inhibitory postsynaptic currents in striosomal cells but not in matrix cells. Disinhibition of cells in the striosomes is further enhanced by inactivation of the protein kinase C cascade. We discuss in this review the possibility that MOR activation in the striosomes affects the activity of cholinergic interneurons and thus leads to changes in synaptic efficacy in the striatum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Gerdeman GL, Partridge JG, Lupica CR et al (2003) It could be habit forming: drugs of abuse and striatal synaptic plasticity. Trends Neurosci 26(4):184–192

    PubMed  CAS  Google Scholar 

  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381

    PubMed  CAS  Google Scholar 

  3. Gerfen CR (1984) The neostriatal mosaic: compartmentalization of corticostriatal input and striatonigral output systems. Nature 311(5985):461–464

    PubMed  CAS  Google Scholar 

  4. Graybiel AM, Ragsdale CW Jr (1978) Histochemically distinct compartments in the striatum of human, monkeys, and cat demonstrated by acetylthiocholinesterase staining. Proc Natl Acad Sci U S A 75(11):5723–5726

    PubMed  CAS  Google Scholar 

  5. Donoghue JP, Herkenham M (1986) Neostriatal projections from individual cortical fields conform to histochemically distinct striatal compartments in the rat. Brain Res 365(2):397–403

    PubMed  CAS  Google Scholar 

  6. Eblen F, Graybiel AM (1995) Highly restricted origin of prefrontal cortical inputs to striosomes in the macaque monkey. J Neurosci 15(9):5999–6013

    PubMed  CAS  Google Scholar 

  7. Ragsdale CW Jr, Graybiel AM (1988) Fibers from the basolateral nucleus of the amygdala selectively innervate striosomes in the caudate nucleus of the cat. J Comp Neurol 269(4):506–522

    PubMed  Google Scholar 

  8. Levesque M, Parent A (1998) Axonal arborization of corticostriatal and corticothalamic fibers arising from prelimbic cortex in the rat. Cereb Cort0ex 8(7):602–613

    CAS  Google Scholar 

  9. Wang H, Pickel VM (1998) Dendritic spines containing mu-opioid receptors in rat striatal patches receive asymmetric synapses from prefrontal corticostriatal afferents. J Comp Neurol 396(2):223–237

    PubMed  CAS  Google Scholar 

  10. Bayer SA (1990) Neurogenetic patterns in the medial limbic cortex of the rat related to anatomical connections with the thalamus and striatum. Exp Neurol 107(2):132–142

    PubMed  CAS  Google Scholar 

  11. Graybiel AM (1990) Neurotransmitters and neuromodulators in the basal ganglia. Trends Neurosci 13(7):244–254

    PubMed  CAS  Google Scholar 

  12. Brown LL, Feldman SM, Smith DM et al (2002) Differential metabolic activity in the striosome and matrix compartments of the rat striatum during natural behaviors. J Neurosci 22(1):305–314

    PubMed  CAS  Google Scholar 

  13. White NM, Hiroi N (1998) Preferential localization of self-stimulation sites in striosomes/patches in the rat striatum. Proc Natl Acad Sci U S A 95(11):6486–6491

    PubMed  CAS  Google Scholar 

  14. Miura M, Saino-Saito S, Masuda M et al (2007) Compartment-specific modulation of GABAergic synaptic transmission by mu-opioid receptor in the mouse striatum with green fluorescent protein-expressing dopamine islands. J Neurosci 27(36):9721–9728

    PubMed  CAS  Google Scholar 

  15. Mansour A, Fox CA, Akil H et al (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18(1):22–29

    PubMed  CAS  Google Scholar 

  16. Pert CB, Kuhar MJ, Snyder SH (1976) Opiate receptor: autoradiographic localization in rat brain. Proc Natl Acad Sci U S A 73(10):3729–3733

    PubMed  CAS  Google Scholar 

  17. Herkenham M, Pert CB (1981) Mosaic distribution of opiate receptors, parafascicular projections and acetylcholinesterase in rat striatum. Nature 291(5814):415–418

    PubMed  CAS  Google Scholar 

  18. Gerfen CR (1992) The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci 15:285–320

    PubMed  CAS  Google Scholar 

  19. Delfs JM, Kong H, Mestek A et al (1994) Expression of mu opioid receptor mRNA in rat brain: an in situ hybridization study at the single cell level. J Comp Neurol 345(1):46–68

    PubMed  CAS  Google Scholar 

  20. Kaneko T, Minami M, Satoh M et al (1995) Immunocytochemical localization of mu-opioid receptor in the rat caudate-putamen. Neurosci Lett 184(3):149–152

    PubMed  CAS  Google Scholar 

  21. Wang H, Cuzon VC, Pickel VM (2003) Postnatal development of mu-opioid receptors in the rat caudate-putamen nucleus parallels asymmetric synapse formation. Neuroscience 118(3):695–708

    PubMed  CAS  Google Scholar 

  22. Winzer-Serhan UH, Chen Y, Leslie FM (2003) Expression of opioid peptides and receptors in striatum and substantia nigra during rat brain development. J Chem Neuroanat 26(1):17–36

    PubMed  CAS  Google Scholar 

  23. Martin-Schild S, Gerall AA, Kastin AJ et al (1999) Differential distribution of endomorphin 1- and endomorphin 2-like immunoreactivities in the CNS of the rodent. J Comp Neurol 405(4):450–471

    PubMed  CAS  Google Scholar 

  24. Zadina JE, Hackler L, Ge LJ et al (1997) A potent and selective endogenous agonist for the mu-opiate receptor. Nature 386(6624):499–502

    PubMed  CAS  Google Scholar 

  25. Arvidsson U, Riedl M, Chakrabarti S et al (1995) Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J Neurosci 15(5 Pt 1):3328–3341

    PubMed  CAS  Google Scholar 

  26. Graybiel AM, Ragsdale CW Jr, Yoneoka ES et al (1981) An immunohistochemical study of enkephalins and other neuropeptides in the striatum of the cat with evidence that the opiate peptides are arranged to form mosaic patterns in register with the striosomal compartments visible by acetylcholinesterase staining. Neuroscience 6(3):377–397

    PubMed  CAS  Google Scholar 

  27. Wang H, Moriwaki A, Wang JB et al (1996) Ultrastructural immunocytochemical localization of mu opioid receptors and Leu5-enkephalin in the patch compartment of the rat caudate-putamen nucleus. J Comp Neurol 375(4):659–674

    PubMed  CAS  Google Scholar 

  28. Wang H, Pickel VM (2001) Preferential cytoplasmic localization of delta-opioid receptors in rat striatal patches: comparison with plasmalemmal mu-opioid receptors. J Neurosci 21(9):3242–3250

    PubMed  CAS  Google Scholar 

  29. Jiang ZG, North RA (1992) Pre- and postsynaptic inhibition by opioids in rat striatum. J Neurosci 12(1):356–361

    PubMed  CAS  Google Scholar 

  30. Barral J, Mendoza E, Galarraga E et al (2003) The presynaptic modulation of corticostriatal afferents by mu-opioids is mediated by K+ conductances. Eur J Pharmacol 462(1–3):91–98

    PubMed  CAS  Google Scholar 

  31. Fishell G, van der Kooy D (1987) Pattern formation in the striatum: developmental changes in the distribution of striatonigral neurons. J Neurosci 7(7):1969–1978

    PubMed  CAS  Google Scholar 

  32. Moon Edley S, Herkenham M (1984) Comparative development of striatal opiate receptors and dopamine revealed by autoradiography and histofluorescence. Brain Res 305(1):27–42

    PubMed  CAS  Google Scholar 

  33. Arlotta P, Molyneaux BJ, Jabaudon D et al (2008) Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J Neurosci 28(3):622–632

    PubMed  CAS  Google Scholar 

  34. Janis LS, Cassidy RM, Kromer LF (1999) Ephrin-A binding and EphA receptor expression delineate the matrix compartment of the striatum. J Neurosci 19(12):4962–4971

    PubMed  CAS  Google Scholar 

  35. Oo TF, Ries V, Cho J et al (2005) Anatomical basis of glial cell line-derived neurotrophic factor expression in the striatum and related basal ganglia during postnatal development of the rat. J Comp Neurol 484(1):57–67

    PubMed  CAS  Google Scholar 

  36. Lopez-Martin E, Caruncho HJ, Rodriguez-Pallares J et al (1999) Striatal dopaminergic afferents concentrate in GDNF-positive patches during development and in developing intrastriatal striatal grafts. J Comp Neurol 406(2):199–206

    PubMed  CAS  Google Scholar 

  37. Nishikawa S, Goto S, Yamada K et al (2003) Lack of Reelin causes malpositioning of nigral dopaminergic neurons: evidence from comparison of normal and Reln(rl) mutant mice. J Comp Neurol 461(2):166–173

    PubMed  CAS  Google Scholar 

  38. van der Kooy D, Fishell G (1987) Neuronal birthdate underlies the development of striatal compartments. Brain Res 401(1):155–161

    PubMed  Google Scholar 

  39. Krushel LA, Fishell G, van der Kooy D (1995) Pattern formation in the mammalian forebrain: striatal patch and matrix neurons intermix prior to compartment formation. Eur J Neurosci 7(6):1210–1219

    PubMed  CAS  Google Scholar 

  40. Krushel LA, Connolly JA, van der Kooy D (1989) Pattern formation in the mammalian forebrain: patch neurons from the rat striatum selectively reassociate in vitro. Brain Res Dev Brain Res 47(1):137–142

    PubMed  CAS  Google Scholar 

  41. Song DD, Harlan RE (1994) Genesis and migration patterns of neurons forming the patch and matrix compartments of the rat striatum. Brain Res Dev Brain Res 83(2):233–245

    PubMed  CAS  Google Scholar 

  42. Matsushita N, Okada H, Yasoshima Y et al (2002) Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J Neurochem 82(2):295–304

    PubMed  CAS  Google Scholar 

  43. Czubayko U, Plenz D (2002) Fast synaptic transmission between striatal spiny projection neurons. Proc Natl Acad Sci U S A 99(24):15764–15769

    PubMed  CAS  Google Scholar 

  44. Tunstall MJ, Oorschot DE, Kean A et al (2002) Inhibitory interactions between spiny projection neurons in the rat striatum. J Neurophysiol 88(3):1263–1269

    PubMed  Google Scholar 

  45. Venance L, Glowinski J, Giaume C (2004) Electrical and chemical transmission between striatal GABAergic output neurones in rat brain slices. J Physiol 559(Pt 1):215–230

    PubMed  CAS  Google Scholar 

  46. Wilson CJ, Groves PM (1980) Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular inject of horseradish peroxidase. J Comp Neurol 194(3):599–615

    PubMed  CAS  Google Scholar 

  47. Bolam JP, Somogyi P, Takagi H et al (1983) Localization of substance P-like immunoreactivity in neurons and nerve terminals in the neostriatum of the rat: a correlated light and electron microscopic study. J Neurocytol 12(2):325–344

    PubMed  CAS  Google Scholar 

  48. Fujiyama F, Fritschy JM, Stephenson FA et al (2000) Synaptic localization of GABA(A) receptor subunits in the striatum of the rat. J Comp Neurol 416(2):158–172

    PubMed  CAS  Google Scholar 

  49. Jaeger D, Kita H, Wilson CJ (1994) Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J Neurophysiol 72(5):2555–2558

    PubMed  CAS  Google Scholar 

  50. Plenz D (2003) When inhibition goes incognito: feedback interaction between spiny projection neurons in striatal function. Trends Neurosci 26(8):436–443

    PubMed  CAS  Google Scholar 

  51. Kita H, Kita T (2001) Number, origins, and chemical types of rat pallidostriatal projection neurons. J Comp Neurol 437(4):438–448

    PubMed  CAS  Google Scholar 

  52. Finnegan TF, Chen SR, Pan HL (2006) Mu opioid receptor activation inhibits GABAergic inputs to basolateral amygdala neurons through Kv1.1/1.2 channels. J Neurophysiol 95(4):2032–2041

    PubMed  CAS  Google Scholar 

  53. Endo K, Yawo H (2000) mu-Opioid receptor inhibits N-type Ca2+ channels in the calyx presynaptic terminal of the embryonic chick ciliary ganglion. J Physiol 524(Pt 3):769–781

    PubMed  CAS  Google Scholar 

  54. Cherubini E, North RA (1985) Mu and kappa opioids inhibit transmitter release by different mechanisms. Proc Natl Acad Sci U S A 82(6):1860–1863

    PubMed  CAS  Google Scholar 

  55. Stefani A, Surmeier DJ, Bernardi G (1994) Opioids decrease high-voltage activated calcium currents in acutely dissociated neostriatal neurons. Brain Res 642(1–2):339–343

    PubMed  CAS  Google Scholar 

  56. Zhu W, Pan ZZ (2005) Mu-opioid-mediated inhibition of glutamate synaptic transmission in rat central amygdala neurons. Neuroscience 133(1):97–103

    PubMed  CAS  Google Scholar 

  57. Vaughan CW, Ingram SL, Connor MA et al (1997) How opioids inhibit GABA-mediated neurotransmission. Nature 390(6660):611–614

    PubMed  CAS  Google Scholar 

  58. Miura M, Watanabe M, Offermanns S et al (2002) Group I metabotropic glutamate receptor signaling via Galpha q/Galpha 11 secures the induction of long-term potentiation in the hippocampal area CA1. J Neurosci 22(19):8379–8390

    PubMed  CAS  Google Scholar 

  59. Tanabe M, Kino Y, Honda M et al (2006) Presynaptic I1-imidazoline receptors reduce GABAergic synaptic transmission in striatal medium spiny neurons. J Neurosci 26(6):1795–1802

    PubMed  CAS  Google Scholar 

  60. Chen XK, Wang LC, Zhou Y et al (2005) Activation of GPCRs modulates quantal size in chromaffin cells through G(betagamma) and PKC. Nat Neurosci 8(9):1160–1168

    PubMed  CAS  Google Scholar 

  61. Ferre S, Ciruela F, Woods AS et al (2007) Functional relevance of neurotransmitter receptor heteromers in the central nervous system. Trends Neurosci 30(9):440–446

    PubMed  CAS  Google Scholar 

  62. Bailey CP, Smith FL, Kelly E et al (2006) How important is protein kinase C in mu-opioid receptor desensitization and morphine tolerance? Trends Pharmacol Sci 27(11):558–565

    PubMed  CAS  Google Scholar 

  63. Walker RH, Arbuthnott GW, Baughman RW et al (1993) Dendritic domains of medium spiny neurons in the primate striatum: relationships to striosomal borders. J Comp Neurol 337(4):614–628

    PubMed  CAS  Google Scholar 

  64. Kawaguchi Y, Wilson CJ, Emson PC (1989) Intracellular recording of identified neostriatal patch and matrix spiny cells in a slice preparation preserving cortical inputs. J Neurophysiol 62(5):1052–1068

    PubMed  CAS  Google Scholar 

  65. Penny GR, Wilson CJ, Kitai ST (1988) Relationship of the axonal and dendritic geometry of spiny projection neurons to the compartmental organization of the neostriatum. J Comp Neurol 269(2):275–289

    PubMed  CAS  Google Scholar 

  66. Bernacer J, Prensa L, Gimenez-Amaya JM (2007) Cholinergic interneurons are differentially distributed in the human striatum. PLoS ONE 2(11):e1174

    PubMed  Google Scholar 

  67. Holt DJ, Graybiel AM, Saper CB (1997) Neurochemical architecture of the human striatum. J Comp Neurol 384(1):1–25

    PubMed  CAS  Google Scholar 

  68. Holt DJ, Hersh LB, Saper CB (1996) Cholinergic innervation in the human striatum: a three-compartment model. Neuroscience 74(1):67–87

    PubMed  CAS  Google Scholar 

  69. Kowall NW, Ferrante RJ, Beal MF et al (1987) Neuropeptide Y, somatostatin, and reduced nicotinamide adenine dinucleotide phosphate diaphorase in the human striatum: a combined immunocytochemical and enzyme histochemical study. Neuroscience 20(3):817–828

    PubMed  CAS  Google Scholar 

  70. Faull RL, Dragunow M, Villiger JW (1989) The distribution of neurotensin receptors and acetylcholinesterase in the human caudate nucleus: evidence for the existence of a third neurochemical compartment. Brain Res 488(1–2):381–386

    PubMed  CAS  Google Scholar 

  71. Jakab RL, Hazrati LN, Goldman-Rakic P (1996) Distribution and neurochemical character of substance P receptor (SPR)-immunoreactive striatal neurons of the macaque monkey: accumulation of SP fibers and SPR neurons and dendrites in "striocapsules" encircling striosomes. J Comp Neurol 369(1):137–149

    PubMed  CAS  Google Scholar 

  72. Prensa L, Gimenez-Amaya JM, Parent A (1999) Chemical heterogeneity of the striosomal compartment in the human striatum. J Comp Neurol 413(4):603–618

    PubMed  CAS  Google Scholar 

  73. Tepper JM, Koos T, Wilson CJ (2004) GABAergic microcircuits in the neostriatum. Trends Neurosci 27(11):662–669

    PubMed  CAS  Google Scholar 

  74. Aosaki T, Kimura M, Graybiel AM (1995) Temporal and spatial characteristics of tonically active neurons of the primate’s striatum. J Neurophysiol 73(3):1234–1252

    PubMed  CAS  Google Scholar 

  75. Graybiel AM, Baughman RW, Eckenstein F (1986) Cholinergic neuropil of the striatum observes striosomal boundaries. Nature 323(6089):625–627

    PubMed  CAS  Google Scholar 

  76. Kubota Y, Kawaguchi Y (1993) Spatial distributions of chemically identified intrinsic neurons in relation to patch and matrix compartments of rat neostriatum. J Comp Neurol 332(4):499–513

    PubMed  CAS  Google Scholar 

  77. Kawaguchi Y, Wilson CJ, Augood SJ et al (1995) Striatal interneurones: chemical, physiological and morphological characterization. Trends Neurosci 18(12):527–535

    PubMed  CAS  Google Scholar 

  78. Aosaki T, Kawaguchi Y (1996) Actions of substance P on rat neostriatal neurons in vitro. J Neurosci 16(16):5141–5153

    PubMed  CAS  Google Scholar 

  79. Bolam JP, Ingham CA, Izzo PN et al (1986) Substance P-containing terminals in synaptic contact with cholinergic neurons in the neostriatum and basal forebrain: a double immunocytochemical study in the rat. Brain Res 397(2):279–289

    PubMed  CAS  Google Scholar 

  80. Kuramoto E, Fujiyama F, Unzai T et al (2007) Metabotropic glutamate receptor 4-immunopositive terminals of medium-sized spiny neurons selectively form synapses with cholinergic interneurons in the rat neostriatum. J Comp Neurol 500(5):908–922

    PubMed  CAS  Google Scholar 

  81. Liu H, Brown JL, Jasmin L et al (1994) Synaptic relationship between substance P and the substance P receptor: light and electron microscopic characterization of the mismatch between neuropeptides and their receptors. Proc Natl Acad Sci U S A 91(3):1009–1013

    PubMed  CAS  Google Scholar 

  82. Miura M, Saino-Saito S, Masuda M et al (2007) Modulation by mu-opioid receptors on the excitability of cholinergic interneuron in the striosome/matrix compartment of the striatum. Soc Neurosci Abstr 514.16/SS30

  83. Stanford IM, Cooper AJ (1999) Presynaptic mu and delta opioid receptor modulation of GABAA IPSCs in the rat globus pallidus in vitro. J Neurosci 19(12):4796–4803

    PubMed  CAS  Google Scholar 

  84. Pakhotin P, Bracci E (2007) Cholinergic interneurons control the excitatory input to the striatum. J Neurosci 27(2):391–400

    PubMed  CAS  Google Scholar 

  85. Miura M, Ishii K, Aosaki T et al (2006) Chronic nicotine treatment increases GABAergic input to striatal neurons. Neuroreport 17(5):537–540

    PubMed  CAS  Google Scholar 

  86. Shen W, Hamilton SE, Nathanson NM et al (2005) Cholinergic suppression of KCNQ channel currents enhances excitability of striatal medium spiny neurons. J Neurosci 25(32):7449–7458

    PubMed  CAS  Google Scholar 

  87. Perez-Rosello T, Figueroa A, Salgado H et al (2005) Cholinergic control of firing pattern and neurotransmission in rat neostriatal projection neurons: role of CaV2.1 and CaV2.2 Ca2+ channels. J Neurophysiol 93(5):2507–2519

    PubMed  CAS  Google Scholar 

  88. Koos T, Tepper JM (2002) Dual cholinergic control of fast-spiking interneurons in the neostriatum. J Neurosci 22(2):529–535

    PubMed  CAS  Google Scholar 

  89. Jabourian M, Venance L, Bourgoin S et al (2005) Functional mu opioid receptors are expressed in cholinergic interneurons of the rat dorsal striatum: territorial specificity and diurnal variation. Eur J Neurosci 21(12):3301–3309

    PubMed  Google Scholar 

  90. Perez S, Tierney A, Deniau JM et al (2007) Tachykinin regulation of cholinergic transmission in the limbic/prefrontal territory of the rat dorsal striatum: implication of new neurokinine 1-sensitive receptor binding site and interaction with enkephalin/mu opioid receptor transmission. J Neurochem 103(6):2153–2163

    PubMed  CAS  Google Scholar 

  91. Kimura M, Rajkowski J, Evarts E (1984) Tonically discharging putamen neurons exhibit set-dependent responses. Proc Natl Acad Sci U S A 81(15):4998–5001

    PubMed  CAS  Google Scholar 

  92. Wilson CJ (2005) The mechanism of intrinsic amplification of hyperpolarizations and spontaneous bursting in striatal cholinergic interneurons. Neuron 45(4):575–585

    PubMed  CAS  Google Scholar 

  93. Aosaki T, Tsubokawa H, Ishida A et al (1994) Responses of tonically active neurons in the primate’s striatum undergo systematic changes during behavioral sensorimotor conditioning. J Neurosci 14(6):3969–3984

    PubMed  CAS  Google Scholar 

  94. Morris G, Arkadir D, Nevet A et al (2004) Coincident but distinct messages of midbrain dopamine and striatal tonically active neurons. Neuron 43(1):133–143

    PubMed  CAS  Google Scholar 

  95. Rice ME, Cragg SJ (2004) Nicotine amplifies reward-related dopamine signals in striatum. Nat Neurosci 7(6):583–584

    PubMed  CAS  Google Scholar 

  96. Zhang H, Sulzer D (2004) Frequency-dependent modulation of dopamine release by nicotine. Nat Neurosci 7(6):581–582

    PubMed  CAS  Google Scholar 

  97. Cragg SJ (2006) Meaningful silences: how dopamine listens to the ACh pause. Trends Neurosci 29(3):125–131

    PubMed  CAS  Google Scholar 

  98. Aosaki T, Graybiel AM, Kimura M (1994) Effect of the nigrostriatal dopamine system on acquired neural responses in the striatum of behaving monkeys. Science 265(5170):412–415

    PubMed  CAS  Google Scholar 

  99. Suzuki T, Miura M, Nishimura K et al (2001) Dopamine-dependent synaptic plasticity in the striatal cholinergic interneurons. J Neurosci 21(17):6492–6501

    PubMed  CAS  Google Scholar 

  100. Reynolds JN, Hyland BI, Wickens JR (2004) Modulation of an afterhyperpolarization by the substantia nigra induces pauses in the tonic firing of striatal cholinergic interneurons. J Neurosci 24(44):9870–9877

    PubMed  CAS  Google Scholar 

  101. Deng P, Zhang Y, Xu ZC (2007) Involvement of I(h) in dopamine modulation of tonic firing in striatal cholinergic interneurons. J Neurosci 27(12):3148–3156

    PubMed  CAS  Google Scholar 

  102. Maurice N, Mercer J, Chan CS et al (2004) D2 dopamine receptor-mediated modulation of voltage-dependent Na+ channels reduces autonomous activity in striatal cholinergic interneurons. J Neurosci 24(46):10289–10301

    PubMed  CAS  Google Scholar 

  103. Wang Z, Kai L, Day M et al (2006) Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron 50(3):443–452

    PubMed  CAS  Google Scholar 

  104. Ferry AT, Ongur D, An X et al (2000) Prefrontal cortical projections to the striatum in macaque monkeys: evidence for an organization related to prefrontal networks. J Comp Neurol 425(3):447–470

    PubMed  CAS  Google Scholar 

  105. Graybiel AM, Saka E (2002) A genetic basis for obsessive grooming. Neuron 33(1):1–2

    PubMed  CAS  Google Scholar 

  106. Graybiel AM, Rauch SL (2000) Toward a neurobiology of obsessive-compulsive disorder. Neuron 28(2):343–347

    PubMed  CAS  Google Scholar 

  107. Graybiel AM, Canales JJ (2001) The neurobiology of repetitive behaviors: clues to the neurobiology of Tourette syndrome. Adv Neurol 85:123–131

    PubMed  CAS  Google Scholar 

  108. Pisani A, Bernardi G, Ding J et al (2007) Re-emergence of striatal cholinergic interneurons in movement disorders. Trends Neurosci 30(10):545–553

    PubMed  CAS  Google Scholar 

  109. The Huntington’s Disease Collaborative Research Group (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington’s disease chromosomes. Cell 72(6):971–983

    Google Scholar 

  110. Tippett LJ, Waldvogel HJ, Thomas SJ et al (2007) Striosomes and mood dysfunction in Huntington’s disease. Brain 130(Pt 1):206–221

    PubMed  Google Scholar 

  111. Lee LV, Maranon E, Demaisip C et al (2002) The natural history of sex-linked recessive dystonia parkinsonism of Panay, Philippines (XDP). Parkinsonism Relat Disord 9(1):29–38

    PubMed  Google Scholar 

  112. Lee LV, Pascasio FM, Fuentes FD et al (1976) Torsion dystonia in Panay, Philippines. Adv Neurol 14:137–151

    PubMed  CAS  Google Scholar 

  113. Kaji R, Goto S, Tamiya G et al (2005) Molecular and anatomical bases of dystonia: X-linked recessive dystonia-parkinsonism (DYT3). Rinsho Shinkeigaku 45(11):811–814

    PubMed  Google Scholar 

  114. Kaji R, Goto S, Tamiya G et al (2005) Molecular dissection and anatomical basis of dystonia: X-linked recessive dystonia-parkinsonism (DYT3). J Med Invest 52(Suppl):280–283

    PubMed  Google Scholar 

  115. Goto S, Lee LV, Munoz EL et al (2005) Functional anatomy of the basal ganglia in X-linked recessive dystonia-parkinsonism. Ann Neurol 58(1):7–17

    PubMed  Google Scholar 

  116. Canales JJ, Graybiel AM (2000) A measure of striatal function predicts motor stereotypy. Nat Neurosci 3(4):377–383

    PubMed  CAS  Google Scholar 

  117. Capper-Loup C, Canales JJ, Kadaba N et al (2002) Concurrent activation of dopamine D1 and D2 receptors is required to evoke neural and behavioral phenotypes of cocaine sensitization. J Neurosci 22(14):6218–6227

    PubMed  CAS  Google Scholar 

  118. Saka E, Goodrich C, Harlan P et al (2004) Repetitive behaviors in monkeys are linked to specific striatal activation patterns. J Neurosci 24(34):7557–7565

    PubMed  CAS  Google Scholar 

  119. Vanderschuren LJ, Schoffelmeer AN, Van Leeuwen SD et al (2002) Compartment-specific changes in striatal neuronal activity during expression of amphetamine sensitization are the result of drug hypersensitivity. Eur J Neurosci 16(12):2462–2468

    PubMed  Google Scholar 

  120. Glickstein SB, Schmauss C (2004) Effect of methamphetamine on cognition and repetitive motor behavior of mice deficient for dopamine D2 and D3 receptors. Ann N Y Acad Sci 1025:110–118

    PubMed  CAS  Google Scholar 

  121. Saka E, Iadarola M, Fitzgerald DJ et al (2002) Local circuit neurons in the striatum regulate neural and behavioral responses to dopaminergic stimulation. Proc Natl Acad Sci U S A 99(13):9004–9009

    PubMed  CAS  Google Scholar 

  122. Balcells-Olivero M, Vezina P (1997) Effects of naltrexone on amphetamine-induced locomotion and rearing: acute and repeated injections. Psychopharmacology (Berl) 131(3):230–238

    CAS  Google Scholar 

  123. Diaz-Otanez CS, Capriles NR, Cancela LM (1997) D1 and D2 dopamine and opiate receptors are involved in the restraint stress-induced sensitization to the psychostimulant effects of amphetamine. Pharmacol Biochem Behav 58(1):9–14

    PubMed  CAS  Google Scholar 

  124. Heidbreder C, Goldberg SR, Shippenberg TS (1993) Inhibition of cocaine-induced sensitization by the delta-opioid receptor antagonist naltrindole. Eur J Pharmacol 243(2):123–127

    PubMed  CAS  Google Scholar 

  125. Hooks MS, Jones DN, Justice JB Jr et al (1992) Naloxone reduces amphetamine-induced stimulation of locomotor activity and in vivo dopamine release in the striatum and nucleus accumbens. Pharmacol Biochem Behav 42(4):765–770

    PubMed  CAS  Google Scholar 

  126. Jones DN, Bowen WD, Portoghese PS et al (1993) Delta-opioid receptor antagonists attenuate motor activity induced by amphetamine but not cocaine. Eur J Pharmacol 249(2):167–177

    PubMed  CAS  Google Scholar 

  127. Jones DN, Holtzman SG (1994) Influence of naloxone upon motor activity induced by psychomotor stimulant drugs. Psychopharmacology (Berl) 114(2):215–224

    CAS  Google Scholar 

  128. Kuzmin AV, Gerrits MA, van Ree JM et al (1997) Naloxone inhibits the reinforcing and motivational aspects of cocaine addiction in mice. Life Sci 60(18):PL-257–PL-264

    CAS  Google Scholar 

  129. Sala M, Braida D, Colombo M et al (1995) Behavioral and biochemical evidence of opioidergic involvement in cocaine sensitization. J Pharmacol Exp Ther 274(1):450–457

    PubMed  CAS  Google Scholar 

  130. Schad CA, Justice JB Jr, Holtzman SG (1996) Differential effects of delta- and mu-opioid receptor antagonists on the amphetamine-induced increase in extracellular dopamine in striatum and nucleus accumbens. J Neurochem 67(6):2292–2299

    Article  PubMed  CAS  Google Scholar 

  131. Schad CA, Justice JB Jr, Holtzman SG (1995) Naloxone reduces the neurochemical and behavioral effects of amphetamine but not those of cocaine. Eur J Pharmacol 275(1):9–16

    PubMed  CAS  Google Scholar 

  132. Woo SK, Hitzemann RJ, Loh HH (1985) Specific opioid-amphetamine interactions in the caudate putamen. Psychopharmacology (Berl) 85(3):371–376

    CAS  Google Scholar 

  133. Horner KA, Keefe KA (2006) Regulation of psychostimulant-induced preprodynorphin, c-fos and zif/268 messenger RNA expression in the rat dorsal striatum by mu opioid receptor blockade. Eur J Pharmacol 532(1–2):61–73

    PubMed  CAS  Google Scholar 

  134. Kawaguchi Y (1992) Large aspiny cells in the matrix of the rat neostriatum in vitro: physiological identification, relation to the compartments and excitatory postsynaptic currents. J Neurophysiol 67(6):1669–1682

    PubMed  CAS  Google Scholar 

Download references

Acknowledgement

This work was supported by grants from the Ministry of Education, Science, Sports, Culture, and Technology of Japan, and from the Smoking Research Foundation of Japan.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Toshihiko Aosaki.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Miura, M., Masuda, M. & Aosaki, T. Roles of μ-Opioid Receptors in GABAergic Synaptic Transmission in the Striosome and Matrix Compartments of the Striatum. Mol Neurobiol 37, 104–115 (2008). https://doi.org/10.1007/s12035-008-8023-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12035-008-8023-2

Keywords

Navigation