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
10.1523/jneurosci.18-01-00266.1998
Crossref journal-article
Society for Neuroscience
The Journal of Neuroscience (393)
Abstract

In vivointracellular spontaneous activity in striatal medium spiny (MS) projection neurons is characterized by “up” and “down” states. How this type of activity relates to the neuronal activity of striatal fast-spiking (FS) interneurons was examined in the presence of nigral and cortical inputs using cortex–striatum–substantia nigra organotypic cultures grown for 45 ± 4 d. The nigrostriatal projection was confirmed by tyrosine hydroxylase immunoreactivity. Corticostriatal (CS) projection neurons, striatal MS neurons, and FS neurons were intracellularly recorded and morphologically and electrophysiologically characterized. Intracellular spontaneous activity in the cultures consisted of intermittent depolarized periods of 0.5–1 sec duration. Spontaneous depolarizations in MS neurons were restricted to a narrow membrane potential range (up state) during which they occasionally fired single spikes. These up states were completely blocked by the glutamate antagonist CNQX. In FS interneurons, depolarized periods were characterized by large membrane potential fluctuations that occupied a wide range between rest and spike threshold. Also, FS interneurons spontaneously fired at much higher rates than did MS neurons. Simultaneous intracellular recordings established that during spontaneous depolarizations MS neurons and FS interneurons displayed correlated subthreshold neuronal activity in the low frequency range. These results indicate that (1) the CS projection neurons, striatal MS neurons, and FS interneurons grown in cortex–striatum–substantia nigra organotypic cultures show morphological and electrophysiological characteristics similar to those seenin vivo; (2) striatal MS neurons but not FS interneurons show an up state; (3) striatal MS neurons and FS interneurons receive common, presumably cortical inputs in the low frequency range. Our results support the view that the cortex provides a feedforward inhibition of MS neuron activity during the up state via FS interneurons.

Bibliography

Plenz, D., & Kitai, S. T. (1998). 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. The Journal of Neuroscience, 18(1), 266–283.

Authors 2
  1. Dietmar Plenz (first)
  2. Stephen T. Kitai (additional)
References 75 Referenced 232
  1. 10.1016/0006-8993(91)91055-6
  2. 10.1007/BF00250260 / Exp Brain Res / Electrotonic properties of neostriatal neurons are modulated by extracellular potassium. by Bargas (1988)
  3. 10.1007/BF00248538 / Exp Brain Res / An early outward conductance modulates the firing latency and frequency of neostriatal neurons of the rat brain. by Bargas (1989)
  4. 10.1016/0006-8993(89)91018-4
  5. 10.1016/0306-4522(94)90471-5
  6. 10.1016/0306-4522(82)90159-2
  7. 10.1016/0306-4522(81)90004-X / Neuroscience / A second type of striatonigral neuron: a comparison between retrogradely labeled and Golgi-stained neurons at the light and electron microscopic levels. by Bolam (1981)
  8. 10.1002/cne.902370102
  9. 10.1016/0306-4522(87)90239-9
  10. 10.1152/jn.1990.63.4.651 / J Neurophysiol / Synaptic and intrinsic control of membrane excitability of neostriatal neurons. I. An in vivo analysis. by Calabresi (1990)
  11. 10.1152/jn.1990.63.4.663 / J Neurophysiol / Synaptic and intrinsic control of membrane excitability of neostriatal neurons. II. An in vitro analysis. by Calabresi (1990)
  12. 10.1113/jphysiol.1991.sp018726
  13. 10.1016/0304-3940(92)90852-X
  14. Calabresi P Mercuri NB Bernardi G (1993) Chemical modulation of synaptic transmission in the striatum. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 299–308. (10.1016/S0079-6123(08)61353-9)
  15. 10.1016/0006-8993(92)90830-3
  16. 10.1126/science.7256286
  17. 10.1002/cne.902080202
  18. 10.1113/jphysiol.1988.sp017143
  19. 10.1152/jn.1994.71.1.17
  20. 10.1007/BF00227194 / Exp Brain Res / Subthreshold rectification in neostriatal spiny projection neurons. by Galarraga (1994)
  21. 10.1016/0165-3806(95)00112-Q
  22. 10.1016/0165-0270(88)90114-8
  23. 10.1152/jn.1994.72.5.2555 / J Neurophysiol / Surround inhibition among projection neurons is weak or nonexistent in the rat neostriatum. by Jaeger (1994)
  24. 10.1113/jphysiol.1991.sp018850
  25. 10.1523/JNEUROSCI.13-11-04908.1993
  26. 10.1152/jn.1989.62.5.1052 / J Neurophysiol / Intracellular recording of identified neostriatal patch and matrix cells in a slice preparation preserving cortical inputs. by Kawaguchi (1989)
  27. 10.1523/JNEUROSCI.10-10-03421.1990 / J Neurosci / Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. by Kawaguchi (1990)
  28. 10.1016/0166-2236(95)98374-8
  29. {'key': '2023041302373082000_18.1.266.29', 'first-page': '911', 'article-title': 'The spacing of synapses along corticostriatal axons.', 'volume': '21', 'author': 'Kincaid', 'year': '1995', 'journal-title': 'Soc Neurosci Abstr'} / Soc Neurosci Abstr / The spacing of synapses along corticostriatal axons. by Kincaid (1995)
  30. Kita H (1993) GABAergic circuits of the striatum. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 51–72. (10.1016/S0079-6123(08)61338-2)
  31. 10.1016/0306-4522(95)00410-6
  32. 10.1016/0165-0270(91)90124-I
  33. 10.1016/0006-8993(88)91138-9
  34. 10.1016/0006-8993(90)90002-S
  35. 10.1016/0006-8993(84)91347-7
  36. 10.1016/0006-8993(85)91246-6
  37. 10.1016/0006-8993(76)90039-1
  38. 10.1007/BF00961434
  39. 10.1016/0006-8993(92)90947-8
  40. 10.1016/0361-9230(83)90058-8
  41. 10.1016/0006-8993(81)90048-2
  42. 10.1002/syn.890080106
  43. {'key': '2023041302373082000_18.1.266.43', 'first-page': '108', 'article-title': 'Depolarizing IPSPs and depolarization by GABA of rat neostriatum cells in vitro.', 'volume': '45', 'author': 'Misgeld', 'year': '1982', 'journal-title': 'Exp Brain Res'} / Exp Brain Res / Depolarizing IPSPs and depolarization by GABA of rat neostriatum cells in vitro. by Misgeld (1982)
  44. 10.1523/JNEUROSCI.15-06-04449.1995
  45. 10.1002/syn.890140306
  46. 10.1152/jn.1994.71.3.1174 / J Neurophysiol / Contribution of a slowly inactivating potassium current to the transition to firing of neostriatal spiny projection neurons. by Nisenbaum (1994)
  47. 10.1007/BF00228796 / Exp Brain Res / Rat ventral mesencephalon grown as organotypic slice cultures and co-cultured with striatum, hippocampus, and cerebellum. by Ostergaard (1990)
  48. 10.1523/JNEUROSCI.17-07-02477.1997
  49. 10.1002/cne.902690211
  50. Plenz D Aertsen A (1994) The basal ganglia: “minimal coherence detection” in cortical activity distributions. in The basal ganglia. IV. New ideas and data on structure and function, eds Percheron G McKenzie JS Feger J (Plenum, New York), pp 579–588. (10.1007/978-1-4613-0485-2_60)
  51. 10.1016/0306-4522(95)00406-8
  52. 10.1016/0306-4522(95)00405-X
  53. 10.1016/0304-3940(96)12644-6
  54. 10.1152/jn.1996.76.6.4180 / J Neurophysiol / Generation of high frequency oscillations in local cortical circuits of rat somatosensory cortex cultures. by Plenz (1996)
  55. Plenz D Wickens J Kitai ST (1996) Basal ganglia control of sequential activity in the cerebral cortex. in Computational neuroscience, ed Bower JM (Academic, San Diego), pp 397–402.
  56. 10.1016/0006-8993(80)90462-X / Brain Res / Medium spiny neuron projection from the rat striatum: an intracellular horseradish peroxidase study. by Preston (1980)
  57. 10.1016/0006-8993(77)90722-3
  58. 10.1016/0006-8993(91)90642-9
  59. 10.1523/JNEUROSCI.14-11-06734.1994
  60. {'key': '2023041302373082000_18.1.266.60', 'first-page': '1087', 'article-title': 'Simultaneous intracellular recording of spontaneous activity in pairs of striatal spiny neurons in vivo.', 'volume': '22', 'author': 'Stern', 'year': '1996', 'journal-title': 'Soc Neurosci Abstr'} / Soc Neurosci Abstr / Simultaneous intracellular recording of spontaneous activity in pairs of striatal spiny neurons in vivo. by Stern (1996)
  61. 10.1152/jn.1997.77.4.1697
  62. Surmeier DJ Kitai ST (1993) D1 and D2 dopamine receptor modulation of sodium and potassium currents in rat neostriatal neurons. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 309–324. (10.1016/S0079-6123(08)61354-0)
  63. 10.1016/0006-8993(88)90334-4
  64. 10.1016/0304-3940(89)90122-5
  65. 10.1016/0304-3940(91)90188-Y
  66. Tepper JM Trent F (1993) In vivo studies of the postnatal development of rat neostriatal neurons. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 35–50. (10.1016/S0079-6123(08)61337-0)
  67. Wickens JR Arbuthnott GW (1993) The cortico-striatal system on computer simulation: an intermediate mechanism for sequencing actions. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 325–340. (10.1016/S0079-6123(08)61355-2)
  68. 10.1002/cne.902630408
  69. Wilson CJ (1992) Dendritic morphology, inward rectification and the functional properties of neostriatal neurons. in Single neuron computation, eds McKenna T Davis J Zornetzer SF (Academic, San Diego), pp 141–170. (10.1016/B978-0-12-484815-3.50012-8)
  70. Wilson CJ (1993) The generation of natural firing patterns in neostriatal neurons. in Progress in brain research: chemical signaling in the basal ganglia, eds Arbuthnott GW Emson PC (Elsevier, Amsterdam), pp 277–298. (10.1016/S0079-6123(08)61352-7)
  71. 10.1002/cne.901940308
  72. 10.1016/0006-8993(81)90211-0
  73. 10.1523/JNEUROSCI.16-07-02397.1996
  74. 10.1523/JNEUROSCI.03-02-00383.1983
  75. 10.1002/cne.901750202
Dates
Type When
Created 7 years, 5 months ago (April 3, 2018, 11:06 a.m.)
Deposited 2 years, 4 months ago (April 13, 2023, 7:46 a.m.)
Indexed 1 month, 2 weeks ago (July 20, 2025, 6:48 p.m.)
Issued 27 years, 8 months ago (Jan. 1, 1998)
Published 27 years, 8 months ago (Jan. 1, 1998)
Published Online 27 years, 8 months ago (Jan. 1, 1998)
Published Print 27 years, 8 months ago (Jan. 1, 1998)
Funders 0

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@article{Plenz_1998, title={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}, volume={18}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.18-01-00266.1998}, DOI={10.1523/jneurosci.18-01-00266.1998}, number={1}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Plenz, Dietmar and Kitai, Stephen T.}, year={1998}, month=jan, pages={266–283} }