When inhibition goes incognito: Feedback interaction between spiny projection neurons in striatal function

Trends in Neurosciences

Volumn 26, Issue 8, 2003, Pages 436-443

  Plenz, Dietmar ^a  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; DOPAMINE; DOPAMINE RECEPTOR; POTASSIUM CHANNEL; 4 AMINOBUTYRIC ACID;

ACTION POTENTIAL; DENDRITIC CELL; FEEDBACK SYSTEM; GABAERGIC TRANSMISSION; GAP JUNCTION; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL PLASTICITY; NERVE CONDUCTION; PRIORITY JOURNAL; REVIEW; STRIATE CORTEX; SYNAPTIC TRANSMISSION; THEORY; ANIMAL; CLASSIFICATION; CORPUS STRIATUM; CYTOLOGY; ELECTROPHYSIOLOGY; NERVE CELL INHIBITION; NERVE CELL NETWORK; PHYSIOLOGY;

ANIMALS; CORPUS STRIATUM; ELECTROPHYSIOLOGY; FEEDBACK, BIOCHEMICAL; GAMMA-AMINOBUTYRIC ACID; NERVE NET; NEURAL INHIBITION; NEURONAL PLASTICITY; NEURONS; SYNAPTIC TRANSMISSION;

EID: 0141996374     PISSN: 01662236     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-2236(03)00196-6     Document Type: Review

References (80)

1. Cajal, S.R.Y. (1911) Histologie du Système Nerveux. A.Maloine, Paris.
2. Vogt C., Vogt O. Zur Lehre der Erkrankungen des striären Systems. J. Psychol. Neurol. 25:1920;627-846.
3. Chang H.T., et al. Single neostriatal efferent axons in the globus pallidus: a light and electron microscopic study. Science. 213:1981;915-918.
4. Kemp J.M., Powell T.P.S. The cortico-striate projection in the monkey. Brain. 93:1970;525-546.
5. DeLong M.R. Putamen: activity of single units during slow and rapid arm movements. Science. 179:1973;1240-1242.
6. Hikosaka O., et al. Functional properties of monkey caudate neurons I. Activities related to saccadic eye movements. J. Neurophysiol. 61:1989;780-798.
7. Jog M.S., et al. Building neural representations of habits. Science. 286:1999;1745-1749.
8. Oertel W.H., Mugnaini E. Immunocytochemical studies of GABAergic neurons in rat basal ganglia and their relationships to other neuronal systems. Neurosci. Lett. 47:1984;233-238.
9. Kita, H. (1993) GABAergic circuits of the Striatum. In Chemical Signaling in the Basal Ganglia (Arbuthnott, G.W. and Emson, P.C., eds), pp. 51-72, Elsevier.
10. Yamada H., et al. Neuronal mechanism underlying dystonia induced by bicuculline injection into the putamen of the cat. Brain Res. 677:1995;333-336.
11. Oorschot D.E. Total number of neurons in the neostriatal, pallidal, subthalamic, and substantia nigra nuclei of the rat basal ganglia: a stereological study using the Cavalieri and optical disector methods. J. Comp. Neurol. 366:1996;580-599.
12. Somogyi P., et al. Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the golgi-peroxidase transport degeneration procedure. J. Comp. Neurol. 195:1981;567-584.
13. Bolam J.P., Izzo P.N. The postsynaptic targets of substance P immunoreactive terminals in the rat neostriatum with particular reference to identified spiny striatonigral neurons. Exp. Brain Res. 70:1988;361-377.
14. Yung K.K., et al. Synaptic connections between spiny neurons of the direct and indirect pathways in the neostriatum of the rat: evidence from dopamine receptor and neuropeptide immunostaining. Eur. J. Neurosci. 8:1996;861-869.
15. Jaeger D., et al. Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. J. Neurophysiol. 72:1994;2555-2558.
16. Fujiyama F., et al. Synaptic localization of GABA(A) receptor subunits in the striatum of the rat. J. Comp. Neurol. 416:2000;158-172.
17. Bolam, J.P. et al. (1983) A type of aspiny neuron in the rat neostriatum accumulates [3H]γ-aminobutyric acid: combination of Golgi-staining, autoradiography, and electron microscopy. J. Comp. Neurol. 213, 121-134.
18. Koos T., Tepper J.M. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 2:1999;467-472.
19. Misgeld U., et al. Depolarizing IPSPs and depolarization by GABA of rat neostriatum cells in vitro. Exp. Brain Res. 45:1982;108-114.
20. Kita T., et al. Local stimulation induced GABAergic response in rat striatal slice preparations: intracellular recordings on QX-314 injected neurons. Brain Res. 360:1985;304-310.
21. Kawaguchi Y., et al. Striatal interneurons: chemical, physiological and morphological characterization. Trends Neurosci. 18:1995;527-535.
22. Plenz D., Kitai S.T. 'Up' and 'down' states in striatal medium spiny neurons simultaneously recorded with spontaneous activity in fast-spiking interneurons studied in cortex-striatum-substantia nigra organotypic cultures. J. Neurosci. 18:1998;266-283.
23. Gerfen, C.R. and Wilson, C.J. (1996) The basal ganglia. In Handbook of Chemical Neuroanatomy 12. Integrated Systems of the CNS, Part III (Swanson, L.W. et al., eds) pp. 371-468, Elsevier Science.
24. Bolam J.P., et al. Synaptic organisation of the basal ganglia. J. Anat. 196:2000;527-542.
25. Groves P.M. A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res. 286:1983;109-132.
26. Wickens J.R., et al. Two dynamic modes of striatal function under dopaminergic-cholinergic control: simulation and analysis of a model. Synapse. 8:1991;1-12.
27. Alexander M.E., Wickens J.R. Analysis of striatal dynamics: the existence of two modes of behaviour. J. Theor. Biol. 163:1993;413-438.
28. Connolly C.I., Burns J.B. A model for the functioning of the striatum. Biol. Cybern. 68:1993;535-544.
29. Wickens J.R., et al. Effects of local connectivity on striatal function: stimulation and analysis of a model. Synapse. 20:1995;281-298.
30. Plenz, D. et al. (1996) Basal ganglia control of sequential activity in the cerebral cortex: a model. In Computational Neuroscience (Bower, J.M., ed.), pp. 397-402, San Diego Academic Press.
31. Fukai T., Tanaka S. A simple neural network exhibiting selective activation of neuronal ensembles: from winner-take-all to winners-share-all. Neural Comput. 9:1997;77-97.
32. Beiser D.G., Houk J.C. Model of cortical-basal ganglionic processing: encoding the serial order of sensory events. J. Neurophysiol. 79:1998;3168-3188.
33. Suri R.E., Schultz W. Learning of sequential movements by neural network model with dopamine-like reinforcement signal. Exp. Brain Res. 121:1998;350-354.
34. Bar-Gad I., Bergman H. Stepping out of the box: information processing in the neural networks of the basal ganglia. Curr. Opin. Neurobiol. 11:2001;689-695.
35. Hartline H.K. Visual receptors and retinal interaction. Science. 164:1969;270-278.
36. Varjú D. Vergleich zweier Modelle für laterale Inhibition. Kyb. 2:1962;200-208.
37. Furman G.G. Comparison of models for subtractive and shunting lateral inhibition in receptor-neuron fields. Kyb. 2:1965;257-274.
38. Von Seelen W. Informationsverarbeitung in homogenen Netzen von Neuronenmodellen. Kyb. 5:1968;133-148.
39. Amari S. A mathematical theory of nerve nets. Adv. Biophys., (Tokyo). 6:1974;75-119.
40. O'Reilly, R.C. (2001) Generalization in interactive networks: the benefits of inhibitory competition and Hebbian learning. Neural Comput. 13, 1199-1241.
41. Thomson A.M. Facilitation, augmentation and potentiation at central synapses. Trends Neurosci. 23:2000;305-312.
42. Thomson A.M. Molecular frequency filters at central synapses. Prog. Neurobiol. 62:2000;159-196.
43. Tunstall M.J., et al. Inhibitory interactions between spiny projection neurons in the rat striatum. J. Neurophysiol. 88:2002;1263-1269.
44. Czubayko U., Plenz D. Fast synaptic transmission between striatal spiny projection neurons. Proc. Natl. Acad. Sci. U.S.A. 99:2002;15764-15769.
45. Wilson C.J., Kawaguchi Y. The origins of two-state spontaneous membrane potential fluctuations of neostriatal spiny neurons. J. Neurosci. 16:1996;2397-2410.
46. Kita H. Glutamatergic and GABAergic postsynaptic responses of striatal spiny neurons to intrastriatal and cortical stimulation recorded in slice preparations. Neuroscience. 70:1996;925-940.
47. Mercuri N.B., et al. GABA depolarizes neurons in the rat striatum: An in vivo study. Synapse. 8:1991;38-40.
48. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat. Rev. Neurosci. 3:2002;728-739.
49. Owens D.F., Kriegstein A.R. Is there more to GABA than synaptic inhibition? Nat. Rev. Neurosci. 3:2002;715-727.
50. Gulledge A.T., Stuart G.J. Excitatory actions of GABA in the cortex. Neuron. 37:2003;299-309.
51. Wilson, C.J. (1992) Dendritic morphology, inward rectification and the functional properties of neostriatal neurons. In Single Neuron Computation (McKenna, T. et al., eds), pp. 141-217, San Diego Academic Press.
52. Nisenbaum E.S., Wilson C.J. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J. Neurosci. 15:1995;4449-4463.
53. Wickens J.R. Striatal dopamine in motor activation and reward-mediated learning: steps towards a unifying model. J. Neural Transm. Gen. Sect. 80:1990;9-31.
54. Suri R.E., Schultz W. A neural network model with dopamine-like reinforcement signal that learns a spatial delayed response task. Neuroscience. 91:1999;871-890.
55. Plenz, D. and Kitai, S.T. (2000) Adaptive classification of cortical input to the striatum by competitive learning. In Brain Dynamics and the Striatal Complex (Miller, R. and Wickens, J.R., eds), pp. 165-177, Harwood Academic Publishers.
56. Fitzpatrick J.S., et al. Short-term plasticity at inhibitory synapses in rat striatum and its effects on striatal output. J. Neurophysiol. 85:2001;2088-2099.
57. Lytton W.W., Sejnowski T.J. Simulations of cortical pyramidal neurons synchronized by inhibitory interneurons. J. Neurophysiol. 66:1991;1059-1079.
58. Oorschot, D.E. et al. (2002) Local connectivity between striatal spiny projection neurons: a re-evaluation. In The Basal Ganglia VII (Nicholson, A.J. and Faull, R.L., eds), pp. 421-434, Kluwer Academic Plenum Publishers.
59. McBain C.J., Fisahn A. Interneurons unbound. Nat. Rev. Neurosci. 2:2001;11-23.
60. Aldridge J.W., Gilman S. The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation. Brain Res. 543:1991;123-138.
61. Calabresi P., et al. Post-receptor mechanisms underlying striatal long-term depression. J. Neurosci. 14:1994;4871-4881.
62. Kerr J.N., Wickens J.R. Dopamine D-1/D-5 receptor activation is required for long-term potentiation in the rat neostriatum in vitro. J. Neurophysiol. 85:2001;117-124.
63. Stuart G.J., Hausser M. Dendritic coincidence detection of EPSPs and action potentials. Nat. Neurosci. 4:2001;63-71.
64. Kerr J.N., Plenz D. Dendritic calcium encodes striatal neuron output during Up-states. J. Neurosci. 22:2002;1499-1512.
65. Reyes A., et al. Target-cell-specific facilitation and depression in neocortical circuits. Nat. Neurosci. 1:1998;279-285.
66. Wickens, J.R. and Arbuthnott, G.W. (1993) The cortico-striatal system on computer simulation: an intermediate mechanism for sequencing actions. In Chemical Signaling in the Basal Ganglia (Arbuthnott, G.W. and Emson, P.C., eds), pp. 325-340, Elsevier.
67. Gupta A., et al. Organizing principles for a diversity of GABAergic interneurons and synapses in the neocortex. Science. 287:2000;273-278.
68. Harsing L.G. Jr, Zigmond M.J. Influence of dopamine on GABA release in striatum: evidence for D1-D2 interactions and non-synaptic influences. Neuroscience. 77:1997;419-429.
69. Delgado A., et al. Inhibitory control of the GABAergic transmission in the rat neostriatum by D2 dopamine receptors. Neuroscience. 95:2000;1043-1048.
70. Czubayko U., Plenz D. Time course, short-term plasticity, and dopamine-dependency of synaptic transmission between striatal spiny projection neurons. Soc. Neurosci. Abstr. 2002;28.164.
71. Guzman J.N., et al. Differential presynaptic modulation of inhibitory inputs to neostriatal projection neurons: dopamine modulates inputs from spiny axon collaterals but not from interneurons. Soc. Neurosci. Abstr. 2002;28.164.
72. Gerfen C.R., et al. D1 and D2 dopamine receptor function in the striatum: Coactivation of D1- and D2-dopamine receptors on separate populations of neurons results in potentiated immediate early gene response in D1-containing neurons. J. Neurosci. 15:1995;8167-8176.
73. Wickens, J.R. (2003) Surround inhibition in the basal ganglia. In The Basal Ganglia VI (DeLong, M.R. and Graybiel, A.M., eds), Plenum.
74. Walsh J.P., et al. Dye-coupling in the neostriatum of the rat: II. Decreased coupling between neurons during development. Synapse. 4:1989;238-247.
75. Cepeda C., et al. Dye-coupling in the neostriatum of the rat: I. Modulation by dopamine- depleting lesions. Synapse. 4:1989;229-237.
76. Onn S.P., Grace A.A. Dye coupling between rat striatal neurons recorded in vivo: compartmental organization and modulation by dopamine. J. Neurophysiol. 71:1994;1917-1934.
77. O'Donnell, P. and Grace, A.A. (1993) Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J. Neurosci. 13, 3456-3471.
78. Kawaguchi Y. Physiological, morphological, and histochemical characterization of three classes of interneurons in rat neostriatum. J. Neurosci. 13:1993;4908-4923.
79. Preston R.J., et al. Medium spiny neuron projection from the rat striatum: an intracellular horseradish peroxidase study. Brain Res. 183:1980;253-263.
80. Wilson C.J., Groves P.M. Fine structure and synaptic connections of the common spiny neuron of the rat neostriatum: a study employing intracellular injection of horseradish peroxidase. J. Comp. Neurol. 194:1980;599-615.