Electrophysiological properties of cholinergic and noncholinergic neurons in the ventral pallidal region of the nucleus basalis in rat brain slices

Journal of Neurophysiology

Volumn 83, Issue 5, 2000, Pages 2649-2660

  Bengtson, C Peter ^a   Osborne, Peregrine B ^a,b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b Prnc of Wales Med Res Institute   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCYTIN; CHOLINE ACETYLTRANSFERASE;

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE CELL; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FOREBRAIN; GLOBUS PALLIDUS; INHIBITORY POSTSYNAPTIC POTENTIAL; MEMBRANE CURRENT; MEMBRANE STEADY POTENTIAL; NEWBORN; NONHUMAN; OLIVARY NUCLEUS; PRIORITY JOURNAL; RAT;

EID: 0034083362     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.5.2649     Document Type: Article

References (77)

1. ALEXANDER, G. E. AND CRUTCHER, M. E. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13: 266-271, 1990.
2. ALEXANDER, G. E., DELONG, M. R., AND STRICK, P. L. Parallel organisation of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9: 357-381, 1986.
3. ALONSO, A., KHATEB, A., FORT, P., JONES, B. E., AND MUHLETHALER, M. Differential oscillatory properties of cholinergic and non-cholinergic nucleus basalis neurons in guinea pig brain slices. Eur. J. Neurosci. 8: 169-182, 1996.
4. BARRY, P. H. JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J. Neurosci. Methods 51: 107-116, 1994.
5. BEVAN, M. D., SMITH, A. D., AND BOLAM, J. P. The substantia nigra as a site of synaptic integration of functionally diverse information arising from the ventral pallidum and the globus pallidus. Neuroscience 75: 5-12, 1996.
6. BOLAM, J. P., INGHAM, C. A., IZZO, P. N., LEVEY, A. I., RYE, D. B., SMITH, A. D., AND WAINER, B. H. 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: 279-289. 1986.
7. f) in guinea-pig dissociated sinoatrial node cells. Br. J. Pharmacol. 110: 343-349, 1993.
8. CARLSEN, J., ZABORSZKY, L., AND HEIMER, L. Cholinergic projections from the basal forebrain to the basolateral amygdaloid complex: a combined retrograde fluorescent and immunohistochemical study. J. Comp. Neurol. 234: 155-167, 1985.
9. DELONG, M. R. AND GEORGOPOULOS, A. P. Motor functions of the basal ganglia. In: Handbook of Physiology. The Nervous System. Motor Control. Bethesda, MD: Am. Physiol. Soc., 1981. sect. 1, vol. II, part 2, p. 1017-1061.
10. DÉTÁRI, L., RASMUSSON, D. D., AND SEMBA, K. The role of basal forebrain neurons in tonic and phasic activation of the cerebral cortex. Prog. Neurobiol. 58: 249-277, 1999.
11. + causes a voltage-dependent block of inward K currents in resting skeletal muscle fibres. Nature 267: 169-170, 1977.
12. GEERAEDTS, L. M., NIEUWENHUYS, R., AND VEENING, J. G. Medial forebrain bundle of the rat. III. Cytoarchitecture of the rostral (telencephalic) part of the medial forebrain bundle bed nucleus. J. Comp. Neurol. 294: 507-536, 1990.
13. GORELOVA, N. AND REINER, P. B. Role of the afterhyperpolarization in control of discharge properties of septal cholinergic neurons in vitro. J. Neurophysiol. 75: 695-706, 1996.
14. GRIFFITH, W. H. Membrane properties of cell types within guinea pig basal forebrain nuclei in vitro. J. Neurophysiol. 59: 1590-1612, 1988.
15. GRIFFITH, W. H. AND MATTHEWS, R. T. Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci. Lett. 71: 169-174, 1986.
16. GRITTI, I., MAINVILLE, L., AND JONES, B. E. Codistribution of GABA-with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J. Comp. Neurol. 329:438-457, 1993.
17. GROENEWEGEN, H. J., BERENDSE, H. W., AND HABER, S. N. Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 57: 113-142, 1993.
18. GROENEWEGEN, H. J., BERENDSE, H. W., WOLTERS, J. G., AND LOHMAN, A. H. The anatomical relationship of the prefrontal cortex with the striatopallidal system, the thalamus and the amygdala: evidence for a parallel organization. Prog. Brain Res. 85: 95-116, 1990.
19. GROVE, E. A. Efferent connections of the substantia innominata in the rat. J. Comp. Neurol. 277: 347-364, 1988.
20. HABER, S. N., GROENEWEGEN, H. J., GROVE, E. A., AND NAUTA, W.J.H. Efferent connections of the ventral pallidum: evidence of a dual striatopallidofugal pathway. J. Comp. Neurol. 235: 322-335, 1985.
21. HABER, S. N., LYND-BALTA, E., AND MITCHELL, S. J. The organization of the descending ventral pallidal projections in the monkey. J. Comp. Neurol. 329: 111-128, 1993.
22. HEIMER, L. AND WILSON, R. D. The subcortical projections of the allocortex: similarities in the neural associations of the hippocampus, the piriform cortex, and the neocortex. In: Gogi Centennial Symposium. New York: Raven, 1975, p. 177-193.
23. HEIMER, L., ZAHM, D. S., CHURCHILL, L., KALIVAS, P. W., AND WOLTHMAN, C. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41: 89-125, 1991.
24. INGHAM, C. A., BOLAM, J. P., WAINER, B. H., AND SMITH, A. D. A correlated light and electron microscopic study of identified cholinergic basal forebrain neurons that project to the cortex in the rat. J. Comp. Neurol. 239: 176-192, 1985.
25. IWAHORI, N. AND MIZUNO, N. A Golgi study on the globus pallidus of the mouse. J. Comp. Neurol. 239: 176-192, 1981.
26. KALIVAS, P. W. Neurotransmitter regulation of dopamine neurons in the ventral tegmental area. Brain Res. Rev. 18: 75-113, 1993.
27. KALIVAS, P. W., CHURCHILL, L., AND ROMANIDES, A. Involvement of the pallidal-thalamocortical circuit in adaptive behavior. Ann. NY Acad. Sci. 877: 64-70, 1999.
28. KHATEB, A., FORT, P., ALONSO, A., JONES, B. E., AND MÜHLETHALER, M. Pharmacological and immunohistochemical evidence for serotonergic modulation of cholinergic nucleus basalis neurons. Eur. J. Neurosci. 5: 541-547, 1993.
29. KHATEB, A., FORT, P., SERAFIN, M., JONES, B. E., AND MÜHLETHALEK, M. Rhythmical bursts induced by NMDA in guinea-pig cholinergic nucleus basalis neurones in vitro. J. Physiol. (Lond.) 487: 623-638, 1995.
30. KHATEB, A., MÜHLETHALER, M., ALONSO, A., SERAFIN, M., MAINVILLE, L., AND JONES, B. E. Cholinergic nucleus basalis neurons display the capacity for rhythmic bursting activity mediated by low-threshold calcium spikes. Neuroscience 51: 489-494, 1992.
31. KITA, H. AND KITAI, S. T. The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res. 636: 308-319, 1994.
32. LAVIN, A. AND GRACE, A. A. Physiological properties of rat ventral pallidal neurons recorded intracellularly in vivo. J. Neurophysiol. 75: 1432-1443, 1996.
33. LEMOAL, M. AND SIMON, H. Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physial. Rev. 71: 155-234, 1991.
34. LUDWIG, A., ZONG, X., JEGLITSCH, M., HOFMANN, F., AND BIEL, M. A family of hyperpolarization-activated mammalian cation channels. Nature 393: 587-591, 1998.
35. LUTHI, A. AND MCCORMICK, D. A. H-current: properties of a neuronal and network pacemaker. Neuron 21: 9-12, 1998.
36. MARKRAM, H, AND SEGAL, M. Electrophysiological characteristics of cholinergic and non-cholinergic neurons in the rat medial septum-diagonal band complex. Brain Res. 513: 171-174, 1990.
37. MAURICE, N., DENIAU, J. M., MENETREY, A., GLOWINSKI, J., AND THIERRY, A. M. Position of the ventral pallidum in the rat prefrontal cortex-basal ganglia circuit. Neuroscience 80: 523-544, 1997.
38. MAYER, M. L. AND WESTBROOK, G. L. A voltage-clamp analysis of inward (anomalous) rectification in mouse spinal sensory ganglion neurones. J. Physiol. (Lond.) 340: 19-45, 1983.
39. MCKINNEY, M., COYLE, J. T., AND HEDREEN, J. C. Topographical analysis of the innervation of the rat neocortex and hippocampus. J. Comp. Neurol. 217: 103-121, 1983.
40. MESULAM, M. M., MUFSON, E. J., WAINER, B. H., AND LEVEY, A. I. Central cholinergic pathways in the rat: an overview based on an alternative no-menclature (Ch1-Ch6). Neuroscience 10: 1185-1201, 1983.
41. MILLHOUSE, O. E. Pallidal neurons in the rat. J. Comp. Neurol. 254: 209-227. 1986.
42. MITROVIC, I. AND NAPIER, T. C. Electrophysiological demonstration of mu, delta and kappa opioid receptors in the ventral pallidum. J. Pharmacol. Exp. Ther. 272: 1260-1270, 1995.
43. MITROVIC, I. AND NAPIER, T. C. Interactions between the mu opioid agonist DAMGO and substance P in regulation of the ventral pallidum. Synapse 23: 142-151, 1996.
44. MOGENSON, G. J., JONES, D. J., AND YIM, C. Y. From motivation to action: functional interface between the limbic system and the motor system. Prog. Neurobiol. 14: 69-97, 1990.
45. NAKANISHI, H., KITA, H., AND KITAI, S. T. Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res. 437: 45-55, 1987.
46. NAKANISHI, H., KITA, H., AND KITAI, S. T. Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: electrical membrane properties. Brain Res. 527: 81-88, 1990.
47. NAKANISHI, H., KITA, H., AND KITAI, S. T. Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: response to subthalamic stimulation. Brain Res. 549: 285-291, 1991.
48. NAMBU, A. AND LLINÁS. R. Electrophysiology of globus pallidus neurons in vitro. J. Neurophysiol. 72: 1127-1139, 1994.
49. NAMBU, A. AND LLINÁS. R. Morphology of globus pallidus neurons: its correlation with electrophysiology in guinea pig brain slices [published erratum appears in 380: 154]. J. Comp. Neurol. 377: 85-94, 1997.
50. NAPIER, T. C. AND MASLOWSKI-COBUZZI, R. J. Electrophysiological verification of the presence of D1 and D2 dopamine receptors within the ventral pallidum. Synapse 17: 160-166, 1994.
51. NAPIER, T. C., SIMSON, P. E., AND GIVENS, B. S. Dopamine electrophysiology of ventral pallidal/substantia innominata neurons: comparison with the dorsal globus pallidus. J. Pharmacol. Exp. Ther. 258: 249-262, 1991.
52. NAUTA, W.J.H., SMITH, G. P., FAULL, R.L.M., AND DOMESIC, V. B. Efferent connections and nigral afferents of the nucleus accumbens septi in the rat. Neuroscience 3: 385-401, 1978.
53. O'DONNEEL, P., LAVIN, A., EVQUIST, L. W., GRACE, A. A., AND CARD, J. P. Interconnected parallel circuits between rat nucleus accumbens and thalamus revealed by retrograde transynaptic transport of pseudorabies virus. J. Neurosci. 17: 2143-2167, 1997.
54. PAGE, K. J. AND SOFRONIEW, M. V. The ascending basal forebrain cholinergic system. Prog. Brain Res. 107: 513-522, 1996.
55. PANG, K., TEPPER, J. M., AND ZABORSZKY, L. Morphological and electrophysiological characteristics of noncholinergic basal forebrain neurons. J. Comp. Neurol. 394: 186-204, 1998.
56. PAPE, H. C. Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Anna. Rev. Physiol. 58: 299-327, 1996.
57. PARENT, A. Identification of the pallidal and peripallidal cells projecting the habenula in monkey. Neurosci. Lett. 15: 159-164, 1979.
58. PARENT, A. AND HAZRATI, L. N. Functional anatomy of the basal ganglia. 1. The cortico-basal ganglia-thalamo-cortical loop. Brain Res. Rev. 20: 91-127, 1995.
59. PARK, M. R., FALLS, W. M., AND KITAI, S. T. An intracellular HRP study of the rat globus pallidus. I. Responses and light microscopic analysis. J. Comp. Neurol. 211: 284-294, 1982.
60. PAXINOS, G. AND WATSON, C. The Rat Brain in Stereotaxic Coordinates (3rd ed.). San Diego, CA: Academic, 1997.
61. RYE, D. B., WAINER, B. H., MESULAM, M. M., MUFSON, E. J., AND SAPER, C. B. Cortical projections arising from the basal forebrain: a study of cholinergic and noncholinergic components employing combined retrograde tracing and immunohistochemical localization of choline acetyltransferase. Neuroscience 13: 627-643, 1984.
62. SAH, P. AND ISAACSON, J. S. Channels underlying the slow afterhyperpolarization in hippocampal pyramidal neurons: neurotransmitters modulate the open probability. Neuron 15: 435-441, 1995.
63. SANTORO, B., LIU, D. T., YAO, H., BARTSCH, D., KANDEL, E. R., SIEGELBAUM, S. A., AND TIBBS, G. R. Identification of a gene encoding a hyperpolarization-activated pacemaker channel of brain. Cell 93: 717-729, 1998.
64. SCHWABER, J. S., ROGERS, W. T., SATOH, K., AND FIBIGER, H. C. Distribution and organization of cholinergic neurons in the rat forebrain demonstrated by computer-aided data acquisition and three-dimensional reconstruction. J. Comp. Neurol. 263: 309-325, 1987.
65. SIM, J. A. AND ALLEN, T.G.J. Morphological and membrane properties of rat magnocellular basal forebrain neurons in cuture. J. Neurophysiol. 80: 1653-1669, 1998.
66. SMITH, Y., BEVAN, M. D., SHINK, E., AND BOLAM, J. P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86: 353-387, 1998.
67. STANDEN, N. B. AND STANFIELD, P. R. A potential- and time-dependent blockade in frog skeletal muscle fibres by barium and strontium ions. J. Phvsiol. (Lond.) 280: 169-191, 1978.
68. 2c receptors, on GABA-mediated synaptic input to rat substantia nigra pars reticulata neurons in vitro. J. Neurosci. 16: 7566-7573, 1996.
69. SWITZER, R. D., HILL, J., AND HEIMER, L. The globus pallidus and its rostroventral extension into the olfactory tubercle of the rat: a cyto- and chemoarchilectural study. Neuroscience 7: 1891-1904, 1982.
70. UCHIMURA, N., CHERUBINI, E., AND NORTH, R. A. Inward rectification in rat nucleus accumbens neurons. J. Neurophysiol. 62: 1280-1286, 1989.
71. Ca currents by internally applied gluconate in rat hippocampal pyramidal neurones. Pflügers Arch. 433: 343-350, 1997.
72. VERNADAKIS, A. AND ROOTS, B. Phylogeny and ontogeny of glial cells. In: Neuron-Glia Interelations During Phylogeny, edited by A. Vernadakis and B. Roots. Totowa, NJ: Humana, 1995, vol. I, p. 276.
73. YELNIK, J., PERCHERON, G., AND FRANCOIS, C. A. Golgi analysis of the primate globus pallidus. II. Quantitative morphology and spatial orientation of dendritic arborizations. J. Comp. Neurol. 227: 200-223, 1984.
74. ZABORSZKY, L. AND CULLMAN, W. F. Projections from the nucleus accumbens to cholinergic neurons of the ventral pallidum: a correlated light and electron microscopic double-immunolabeling study in rat. Brain Res. 570: 92-101, 1992.
75. ZABORSZKY, L., LERANTH, C., AND HEIMER, L. Ultrastructural evidence of amygdalofugal axons terminating on cholinergic cells of the rostral forebrain. Neurosci. Lett. 52: 219-225, 1984.
76. ZAHM, D. S. AND HEIMER, L. Two transpallidal pathways originating in the rat nucleus accumbens. J. Comp. Neurol. 302: 437-446, 1990.
77. ZAHM, D. S., WILLIAMS, E., AND WOHLTMANN, C. Ventral striatopallidothalamic projection. IV. Relative involvements of neurochemically distinct subterritories in the ventral pallidum and adjacent parts of the rostroventral forebrain. J. Comp. Neurol. 364: 340-362, 1996.