Simultaneous release of glutamate and acetylcholine from single magnocellular "cholinergic" basal forebrain neurons

Journal of Neuroscience

Volumn 26, Issue 5, 2006, Pages 1588-1595

  Allen, Timothy G J ^a   Abogadie, Fe C ^a   Brown, David A ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Acetylcholine (ACh); Basal forebrain; Cholinergic neuron; Glutamate; Neurotransmitter; Presynaptic regulation

Indexed keywords

ACETYLCHOLINE; CHOLINESTERASE; GLUTAMIC ACID; HEXAMETHONIUM; KYNURENIC ACID; METABOTROPIC RECEPTOR; MUSCARINIC M2 RECEPTOR; NEOSTIGMINE; NICOTINE; NICOTINIC RECEPTOR; PIRENZEPINE; TRIPITRAMINE;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; BRAIN NERVE CELL; CELL CULTURE; CELL STIMULATION; CHOLINERGIC NERVE CELL; CONCENTRATION RESPONSE; CONTROLLED STUDY; FOREBRAIN; LATENT PERIOD; NEGATIVE FEEDBACK; NEURITE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SYNAPSE; VOLTAGE CLAMP;

ACETYLCHOLINE; ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; GLUTAMIC ACID; NEURAL INHIBITION; NEURONS; PATCH-CLAMP TECHNIQUES; PROSENCEPHALON; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, MUSCARINIC M2; RECEPTORS, GLUTAMATE; RECEPTORS, PRESYNAPTIC; SYNAPSES;

EID: 32544439510     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3979-05.2006     Document Type: Article

References (56)

1. 2+ channels in feedback inhibition of ACh release from rat basal forebrain neurons. J Physiol (Lond) 515:93-107.
2. 2+ current in rat magnocellular cholinergic basal forebrain neurones. J Physiol (Lond) 466:173-189.
3. Allen TGJ, Brown DA (1996) Detection and modulation of acetylcholine release from neurites of rat basal forebrain cells in culture. J Physiol (Lond) 492:453-466.
4. Allen TGJ, Brown DA (2004) Modulation of the excitability of cholinergic basal forebrain neurones by KATP channels. J Physiol (Lond) 554:353-370.
5. Beaulieu C, Somogyi P (1991) Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J Comp Neurol 304:666-680.
6. Bekkers JM, Stevens CF (1991) Excitatory and inhibitory autaptic currents in isolated hippocampal neurons maintained in cell culture. Proc Natl Acad Sci USA 88:7834-7838.
7. Benardo LS, Prince DA (1982) Cholinergic pharmacology of mammalian hippocampal pyramidal cells. Neuroscience 7:1703-1712.
8. Burnstock G (2004) Cotransmission. Curr Opin Pharmacol 4:47-52.
9. Caulfield MP, Birdsall NJ (1998) International Union of Pharmacology. XVII. Classification of muscarinic acetylcholine receptors. Pharmacol Rev 50:279-290.
10. Cole AE, Nicoll RA (1984) Characterization of a slow cholinergic postsynaptic potential recorded in vitro from rat hippocampal pyramidal cells. J Physiol (Lond) 352:173-188.
11. Coyle JT, Price DL, DeLong MA (1983) Alzheimer's disease: a disorder of cortical cholinergic innervation. Science 219:1184-1190.
12. 3H]D-aspartate autoradiography. Neuroscience 101:637-655.
13. Csaki A, Kocsis K, Kiss J, Halasz B (2002) Localization of putative glutamatergic/aspartatergic neurons projecting to the supraoptic nucleus area of the rat hypothalamus. Eur J Neurosci 16:55-68.
14. Docherty M, Bradford HF, Wu J-Y (1987) Co-release of glutamate and aspartate from cholinergic and GABAergic synaptosomes. Nature 330:64-66.
15. Dudar JD, Szerb JC (1969) The effect of topically applied atropine on resting and evoked cortical acetylcholine release. J Physiol (Lond) 203:741-762.
16. Fremeau Jr RT, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EF, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247-260.
17. Furuta T, Koyano K, Tomioka R, Yanagawa Y, Kaneko TK (2004) GABAergic basal forebrain neurons that express receptor for neurokinin B and send axons to the cerebral cortex. J Comp Neurol 473:43-58.
18. Gahwiler BH, Brown DA (1985) Functional innervation of cultured hippocampal neurones by cholinergic afferents from co-cultured septal explants. Nature 313:577-579.
19. Gritti I, Mainville L, Jones BF (1993) Codistribution of GABA- with acetylcholine-synthesizing neurons in the basal forebrain of the rat. J Comp Neurol 329:438-457.
20. Gritti I, Mainville L, Mancia M, Jones BF (1997) GABAergic and other non-cholinergic basal forebrain neurons, together with cholinergic neurons, project to the mesocortex and isocortex in the rat. J Comp Neurol 383:163-177.
21. Gritti I, Manns ID, Mainville L, Jones BF (2003) Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J Comp Neurol 458:11-31.
22. Haas HL (1982) Cholinergic disinhibition in hippocampal slices of the rat. Brain Res 233:200-204.
23. Hajszan T, Alreja M, Leranth C (2004) Intrinsic vesicular glutamate transporter 2-immunoreactive input to septohippocampal parvalbumin-containing neurons: novel glutamatergic local circuit cells. Hippocampus 14:499-509.
24. Harkany T, Mulder J, Sasvari M, Abraham I, Konya C, Zarandi M, Penke B, Luiten PG, Nyakas C (1999) N-methyl-D-aspartate receptor antagonist MK-801 and radical scavengers protect cholinergic nucleus basalis neurons against beta-amyloid neurotoxicity. Neurobiol Dis 6:109-121.
25. Israel M, Lesbats B, Bruner J (1993) Glutamate and acetylcholine release from cholinergic nerve terminals, a calcium control of the specificity of the release mechanism. Neurochem Int 22:53-58.
26. 3H]D-aspartate labelling and immunocytochemistry. Neuroscience 111:671-691.
27. Landis SC (1976) Rat sympathetic neurons and cardiac myocytes developing in microcultures: correlation of the fine structure of endings with neurotransmitter function in single neurons. Proc Natl Acad Sci USA 73:4220-4224.
28. Leranth C, Frotscher M (1989) Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J Comp Neurol 289:304-314.
29. Li WC, Soffe SR, Roberts A (2004) Glutamate and acetylcholine corelease at developing synapses. Proc Natl Acad Sci USA 101:15488-15493.
30. Lin W, McKinney K, Liu L, Lakhlani S, Jennes L (2003) Distribution of vesicular glutamate transporter-2 messenger ribonucleic acid and protein in the septum-hypothalamus of the rat. Endocrinology 144:662-670.
31. Lucas-Meunier E, Fossier P, Baux G, Amar M (2003) Cholinergic modulation of the cortical neuronal network. Pflügers Arch 446:17-29.
32. Manns ID, Mainville L, Jones BF (2001) Evidence for glutamate, in addition to acetylcholine and GABA, neurotransmitter synthesis in basal forebrain neurons projecting to the entorhinal cortex. Neuroscience 107:249-263.
33. Manns ID, Alonso A, Jones BF (2003) Rhythmically discharging basal forebrain units comprise cholinergic, GABAergic, and putative glutamatergic cells. J Neurophysiol 89:1057-1066.
34. Mennerick SJ, Que J, Benz A, Zorumski CF (1995) Passive and synaptic properties of hippocampal neurons grown in microcultures and in mass cultures. J Neurophysiol 73:320 -332.
35. Mentis GZ, Alvarez FJ, Bonnot A, Richards DS, Gonzales-Forero D, Zerda R, O'Donovan MJ (2005) Noncholinergic excitatory actions of motoneurons in the neonatal mammalian spinal cord. Proc Natl Acad Sci USA 102:7344-7349.
36. Mesulam MM, Mufson EJ, Wainer BH, Levey AI (1983) Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1-Ch6). Neuroscience 10:1185-1201.
37. Mrzljak L, Pappy M, Leranth C, Goldman-Rakic PS (1995) Cholinergic synaptic circuitry in the macaque prefrontal cortex. J Comp Neurol 357:603-617.
38. Nishimura H, Restrepo CE, Rynge JY, Kiehn O (2005) Mammalian motor neurons corelease glutamate and acetylcholine at central synapses. Proc Natl Acad Sci USA 102:5245-5249.
39. Page KJ, Everitt BJ (1995) The distribution of neurons coexpressing immunoreactivity to BMPA-sensitive glutamate receptor subtypes (GluR1-4) and nerve growth factor receptor in the rat basal forebrain. Eur J Neurosci 7:1022-1033.
40. Perry EK, Tomlinson BE, Blessed G, Bergmann K, Gibsoa PH, Perry RH (1978) Correlation of cholinergic abnormalities with senile plaque and mental test scores in senile dementia. Br Med J 2:1457-1459.
41. Pfrieger FW, Gottmann K, Lux HD (1994) Kinetics of GABAB receptor-mediated inhibition of calcium currents and excitatory synaptic transmission in hippocampal neurons in vitro. Neuron 12:97-107.
42. Potter DD, Landis SC, Furshpan EJ (1980) Dual function during development of rat sympathetic neurones in culture. J Exp Biol 89:57-71.
43. Price JL, Stern R (1983) Individual cells in the nucleus basalis-diagonal band complex have restricted axonal projections to the cerebral cortex in the rat. Brain Res 269:352-356.
44. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26.
45. Segal MM (1991) Epileptiform activity in microcultures containing one excitatory hippocampal neuron. J Neurophysiol 65:761-770.
46. Sim JA, Allen TGJ (1998) Morphological and membrane properties of rat magnocellular basal forebrain neurons maintained in culture. J Neurophysiol 80:1653-1669.
47. Sim JA, Griffith WH (1996) Muscarinic inhibition of glutamatergic transmissions onto rat magnocellular basal forebrain neurons in a thin-slice preparation. Eur J Neurosci 8:880-891.
48. Sotty F, Danik M, Manseau F, Laplante F, Quirion R, Williams SM (2003) Distinct electrophysiological properties of glutamatergic, cholinergic and GABAergic rat septohippocampal neurons: novel implications for hippocampal rhythmicity. J Physiol (Lond) 551:927-943.
49. Umbriaco D, Watkins KC, Descarries L, Cozzari C, Hartman BK (1994) Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J Comp Neurol 348:351-373.
50. 2+-permeable non-NMDA glutamate receptors in rat magnocellular basal forebrain neurons. J Physiol (Lond) 508:453-469.
51. Wenk GL (1997) The nucleus basalis magnocellularis cholinergic system: one hundred years of progress. Neurobiol Learn Mem 67:85-95.
52. Whitehouse PJ, Price DL, Struble RG, Clark AW, Cotle JT, DeLong MR (1982) Alzheimers disease and senile dementia: loss of neurons in the basal forebrain. Science 215:1237-1239.
53. Yamada KA, Tang CM (1993) Benzothiadiazides inhibit rapid glutamate receptor desensitization and enhance glutamatergic synaptic currents. J Neurosci 13:3904-3915.
54. Zaborszky L, Carlsen J, Brashear HR, Heimer L (1986) Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J Comp Neurol 243:488-509.
55. Zaborszky L, Pang K, Somogyi J, Nadazdy Z, Kallo I (1999) The basal forebrain corticopetal system revisited. Ann NY Acad Sci 877:339-367.
56. 2+ channel modulation by neurotransmitters in rat sympathetic neurons. J Neurophysiol 77:2040-2048.