Dopamine modulation of membrane and synaptic properties of interneurons in rat cerebral cortex

Journal of Neurophysiology

Volumn 81, Issue 3, 1999, Pages 967-976

  Zhou, Fu Ming ^a,b   Hablitz, John J ^a  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; DOPAMINE;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ARTICLE; BRAIN CELL; BRAIN CORTEX; DENDRITIC SPINE; DEPOLARIZATION; DOPAMINERGIC TRANSMISSION; HYPERPOLARIZATION; INHIBITORY POSTSYNAPTIC POTENTIAL; INNERVATION; INTERNEURON; NERVE EXCITABILITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC MEMBRANE;

EID: 0033018297     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.1999.81.3.967     Document Type: Article

References (64)

1. AKBARIAN, S., KIM, J. J., POTKIN, S. G., HAGMAN, J. O., TAFAZZOLI, A., BUNNEY, W. E., JR., AND JONES, E. G. Gene expression for glutamic acid decarboxylase is reduced without loss of neurons in prefrontal cortex of schizophrenics. Arch. Gen. Psychiatry 52: 258-266, 1995.
2. ANDREASON, N. C. Pieces of the schizophrenia puzzle fall into place. Neuron 16: 697-700, 1996.
3. BENARDO, L. S. AND PRINCE, D. A. Dopamine action on hippocampal pyramidal cells. J. Neurosci. 2: 415-423, 1982.
4. A receptor binding on neurons of the prefrontal cortex in schizophrenic subjects. Neuroscience 75: 1021-1031, 1996.
5. BENES, F. M., VINCENT, S. L., AND MOLLOY, R. Dopamine-immunoreactive axon varicosities form non-random contacts with GABA-immunoreactive neurons of rat medial prefrontal cortex. Synapse 15: 285-295, 1993.
6. BERGER, B. Dopaminergic innervation of the frontal cerebral cortex: evolutionary trends and functional implications. In: Advances in Neurology. Frontal Lobe Seizures and Epilepsies, edited by P. Chauvel, A. V. Delgado-Escueta, E. Halgren, and J. Bancaud. New York: Raven, 1992, vol. 57, p. 525-544.
7. BERGSON, C., MRZLJAK, L., SMILEY, J., PAPPY, M., LEVENSON, R., AND GOLDMAN-RAKIC, P. S. Regional, cellular, and subcellular variations in the distribution of D1 and D5 dopamine receptors in the primate brain. J. Neurosci. 15: 7821-7836, 1995.
8. BERRETTA, N., BERTON, F., BIANCHI, R., CAPOGNA, M., FRANCESCONI, W., AND BRUNELLI, M. Effects of dopamine, D-1 and D-2 dopaminergic agonists on the excitability of hippocampal CA1 pyramidal cells in guinea pig. Exp. Brain Res. 83: 124-130, 1990.
9. BJORKLUND, A. AND LINDVALL, O. Catecholaminergic brain stem regulatory systems. In: Handbook of Physiology. The Nervous System. Washington, DC: Am. Physiol. Soc., 1986, sect. 1, p. 155-235.
10. BOYSON, S. J., MCGONIGLE, P., AND MOLNOFF, P. B. Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in the rat brain. J. Neurosci. 6: 3177-3188, 1986.
11. BUNNEY, B. S. AND CHIODO, L. A. Mesocortical dopamine systems: further electrophysiological and pharmacological characteristics. In: Monoamine Innervation of Cerebral Cortex, edited by L. Descarries, T. R. Reader, and H. H. Jasper. New York: Liss, 1984, p. 263-277.
12. CREESE, I., BURT, D. R., AND SNYDER, S. H. Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 192:481-483, 1976.
13. DESCARRIES, L., SEQUELA, P., AND WATKINS, K. C. Nonjunctional relationships of monoamine axon terminals in the cerebral cortex of adult rat. In: Volume Transmission in the Brain, edited by K. Fuxe and L. F. Agnati. New York: Raven, 1991, p. 49-62.
14. DESCARRIES, L. AND UMBRIACO, D. Ultrastructural basis of monoamine and acetycholine function in CNS. Semin. Neurosci. 7: 309-318, 1995.
15. DOLAN, R. J., FLETCHER, P., FRITH, C. D., FRISTON, K. J., FRACKOWIAK, R.S.J., AND GRASVY, P. M. Dopaminergic modulation of impaired cognitive activation in the anterior cingulate cortex in schizophrenia. Nature 378: 180-182, 1995.
16. EDWARDS, F. A., KONNERTH, A., SAKMANN, B., AND TAKAHASHI, T. A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflügers Arch. 414: 600-612, 1989.
17. EGAN, M. F. AND WEINBERGER, D. Neurobiology of schizophrenia. Curr. Opin. Neurobiol. 3: 701-707, 1997.
18. GABBOTT, P.L.A. AND SOMOGYI, P. Quantitative distribution of GABA-immunoreactive neurons in the visual cortex (area 17) of the cat. Exp. Brain Res. 61: 323-331, 1986.
19. GELLMAN, R. L. AND AGHAJANIAN, G. K. Pyramidal cells in piriform cortex receive a convergence of inputs from monoamine activated GABAergic interneurons. Brain Res. 600: 63-73, 1993.
20. GOLDMAN-RAKIC, P. S. Dopamine-mediated mechanisms of the prefrontal cortex. Semin. Neurosci. 4: 149-159, 1992.
21. GOLDMAN-RAKIC, P. S., LERANTH, C., WILLIAMS, S. M., MONS, N., AND GEFFARD, M. Dopamine synaptic complex with pyramidal neurons in primate cerebral cortex. Proc, Natl. Acad. Sci. USA 86: 9015-9019, 1989.
22. GRACE, A. A., BUNNEY, B. S., MOORE, H., AND TODD, C. L. Dopamine-cell depolarization as a model for the therapeutic actions of antipsychotic drugs. Trends Neurosci. 20: 31-37, 1997.
23. HARDINGHAM, N. R. AND LARKMAN, A. U. The reliability of excitatory synaptic transmission in slices of rat visual cortex in vitro is temperature dependent. J. Physiol. (Lond.) 507: 249-256, 1998.
24. JASKIW, G. E. AND WEINBERGER, D. Dopamine and schizophrenia - a cortically corrective perspective. Semin. Neurosci. 4: 179-188, 1992.
25. KEBABIAN, J. W. AND CALNE, D. B. Multiple receptors for dopamine. Nature 277: 93-96, 1979.
26. KRIMER, L. S., JAKAB, R. L., AND GOLDMAN-RAKIC, P. S. Quantitative three-dimensional analysis of the Catecholaminergic innervation of identified neurons in the macaque prefrontal cortex. J. Neurosci. 17: 7450-7461, 1997.
27. KOLB, B. Organization of the neocortex of the rat. In: The Cerebral Cortex of the Rat, edited by B. Kolb and R. C. Tees. Cambridge, MA: MIT Press, 1990, p. 21-33.
28. MCCORMICK, D. A., CONNORS, B. W., LIGHTHALL, J. W., AND PRINCE, D. A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J. Neurophysiol. 54: 782-806, 1985.
29. MICHEVA, K. D. AND BEAULIEU, C. Quantitative aspects of synaptogenesis in the rat barrel filed cortex with special reference to GABA circuitry. J. Comp. Neurol 373: 340-354, 1996.
30. MISSALE, C., NASH, S. R., ROBINSON, S. W., JABER, M., AND CARON, M. G. Dopamine receptors: from structure to function. Physiol. Rev. 78: 189-225, 1998.
31. MRZLJAK, L., BERGSON, C., PAPPY, M., HUFF, R., LEVENSON, R., AND GOLDMAN-RAKIC, P. S. Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 381: 245-248, 1996.
32. NESTLER, E. J. An emerging pathophysiology. Nature 385: 578-579, 1997.
33. NICOLA, S. M. AND MALENKA, R. C. Dopamine depresses excitatory and inhibitory synaptic transmission by distinct mechanisms in the nucleus accumbens. J. Neurosci. 17: 5697-5710, 1997.
34. OKUBO, Y., SUHARA, T., SUZUKI, K., KOBAYASHI, K., INOUE, O., TERASAKI, O., SOMEYA, Y., SASSA, T., SUDO, Y., MATSUSHIMA, E., IYO, M., TATENO, Y., AND TORU, M. Decreased prefrontal dopamine D1 receptors in schizophrenia revealed by PET. Nature 385: 634-636, 1997.
35. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates (2nd ed.). Sydney, Australia: Academic, 1986.
36. PENIT-SORIA, J., AUDINAT, E., AND CREPEL, F. Excitation of rat prefrontal cortical neurons by dopamine: an in vitro electrophysiological study. Brain Res. 425: 263-274, 1987.
37. PETERS, A. Number of neurons and synapses in primary visual cortex. In: Cerebral Cortex, edited by E. G. Jones and A. Peters. New York: Plenum, 1987, vol. 6, p. 267 and 294.
38. PIROT, S., GODBOUT, R., MANTZ, J., TASSIN, J.-P., GLOWINSKI, J., AND THIERRY, A.-M. Inhibitory effects of ventral tegmental area stimulation on the activity of prefrontal cortical neurons: evidence for the involvement of both dopaminergic and GABAergic components. Neuroscience 49: 857-865, 1992.
39. SAWAGUCHI, T., MATSUMURA, M., AND KUBOTA, K. Catecholamine sensitivities of motor cortical neurons of the monkey. Neurosci. Lett. 66: 135-140, 1986.
40. SESACK, S. R. AND BUNNEY, B. S. Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: a microiontophoretic study. J. Pharmacol. Exp. Ther. 248: 1323-1333, 1989.
41. SESACK, S. R., SNYDER, C. L., AND LEWIS, D. Axon terminals immunolabeled for dopamine or tyrosine hydroxylase synapse on GABA-immunoreactive dendrites in rat and monkey cortex. J. Camp. Neurol. 363: 264-280, 1995.
42. SHI, W. X., ZHENG, P., LIANG, X. E., AND BUNNEY, B. S. Characterization of dopamine-induced depolarization of prefrontal cortical neurons. Synapse 26: 415-422, 1997.
43. SMIALOWSKI, A. AND BUAK, M. Excitatory and inhibitory action of dopamine on hippocampal neurons in vitro. Involvement of D2 and D1 receptors. Neuroscience 23: 95-101, 1987.
44. SMILEY, J. F. AND GOLDMAN-RAKIC, P. S. Heterogeneous targets of dopamine synapses in monkey prefrontal cortex demonstrated by serial section electron microscopy: a laminar analysis using the silver-enhanced diaminobenzidine sulfide (SEDS) immunolabeling technique. Cerebral Cortex 3: 223-238, 1993.
45. SMILEY, J. F., LEVEY, A. I., CILIAX, B. J., AND GOLDMAN-RAKIC, P. S. D1 dopamine receptor immunoreactivity in human and monkey cerebral cortex: predominant and extrasynaptic localization in dendritic spines. Proc. Natl. Acad. Sci. USA 91: 5720-5724, 1994.
46. SMILEY, J. F., WILLIAMS, S. M., SZIGETI, L., AND GOLDMAN-RAKIC, P. S. Light and electron microscopic characterization of dopamine-immunoreactive processes in human cerebral cortex. J. Comp. Neurol. 321: 325-335, 1992.
47. STARR, M. S. The role of dopamine in epilepsy. Synapse 22: 159-194, 1996.
48. SUTOR, B. AND HABLITZ, J. J. EPSPs in rat neocortical neurons in vitro I. Electrophysiological evidence for two distinct EPSPs. J. Neurophysiol. 61: 607-620, 1989.
49. SUTOR, B. AND TEN BRUGGENCATE, G. Ascorbic acid: a useful reductant to avoid oxidation of catecholamines in electrophysiological experiments in vitro? Neurosci. Lett. 116: 287-292, 1990.
50. THIERRY, A. M., BLANC, G., SOBEL, A., STINUS, L., AND GLOWINSKI, J. Dopaminergic terminals in the rat cortex. Science 182: 499-501, 1973.
51. THIERRY, A. M., MANTZ, J., AND GLOWINSKI, J. Influence of dopaminergic and noradrenergic afferents on their target cells in the rat medial prefrontal cortex. In: Advances in Neurology. Frontal Lobe Seizures and Epilepsies, edited by P. Chauvel, A. V. Delgado-Escueta, E. Halgren, and J. Bancaud. New York: Raven, 1992, vol. 57, p. 545-554.
52. TRIMBLE, M. R. Biological Psychiatry (2nd ed.). West Sussex, UK: Wiley, 1996.
53. UCHIMURA, N., HIGASHI, H., AND NISHI, S. Hyperpolarizing and depolarizing actions of dopamine via D-1 and D-2 receptors on nucleus accumbens neurons. Brain Res. 375: 368-372, 1986.
54. VERNEY, C., ALVAREZ, C., GEFFARD, M., AND BERGER, B. Ultrastructural double labeling study of dopamine terminals and GABA-containing neurons in rat anteromedial cerebral cortex. Eur. J. Neurosci. 2: 295-298, 1990.
55. VINCENT, S. L., KHAN, Y., AND BENES, F. M. Cellular distribution of dopamine D1 and D2 receptors in rat medial prefrontal cortex. J. Neurosci. 13: 2551-2564, 1993.
56. VINCENT, S. L., KHAN, Y., AND BENES, F. M. Cellular colocalization of dopamine D1 and D2 receptors in rat medial prefrontal cortex. Synapse 19: 112-120, 1995.
57. WEINBERGER, D. AND BERMAN, K. F. Prefrontal function in schizophrenia: confounds and controversies. Trans. R. Soc. Lond. B 351: 1495-1503, 1996.
58. WILLIAMS, G. V. AND GOLDMAN-RAKIC, P. S. Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376: 572-575, 1995.
59. WILLIAMS, S. M. AND GOLDMAN-RAKIC, P. S. Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cereb. Cortex 3: 199-222, 1993.
60. YANG, C. R. AND SEAMANS, J. K. Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendritic-somatic signal integration. J. Neurosci. 16: 1922-1935, 1996.
61. ZHOU, F.-M. AND HABLITZ, J. J. Rat neocortical layer I neurons. I. Action potential and repetitive firing properties. J. Neurophysiol. 76: 651-667, 1996.
62. ZHOU, F.-M. AND HABLITZ, J. J. Rapid kinetics and inward rectification of miniature EPSCs in layer I neurons of rat neocortex. J. Neurophysiol. 77: 2416-2426, 1997a.
63. ZHOU, F.-M. AND HABLITZ, J. J. Metabotropic glutamate receptor enhancement of spontaneous IPSCs in neocortical interneurons. J. Neurophysiol. 78: 2287-2295, 1997b.
64. ZHOU, F.-M. AND HABLITZ, J. J. Direct excitation of cortical interneurons by metabotropic glutamate receptors. Soc Neurosci. Abstr. 23: 2025, 1997c.