Group I metabotropic glutamate receptor activation produces a direct excitation of identified septohippocampal cholinergic neurons

Journal of Neurophysiology

Volumn 92, Issue 2, 2004, Pages 1216-1225

  Wu, Min ^a   Hajszan, Tibor ^a,b   Xu, Changqing ^a   Leranth, Csaba ^a   Alreja, Meenakshi ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF BIOCHEMISTRY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; 3,5 DIHYDROXYPHENYLGLYCINE; 4 AMINOBUTYRIC ACID RECEPTOR; 4 CARBOXY 2 METHYLPHENYLGLYCINE; 7 HYDROXIMINOCYCLOPROPAN[B]CHROMEN 1A CARBOXYLIC ACID ETHYL ESTER; ACETYLCHOLINE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR AGONIST; METABOTROPIC RECEPTOR ANTAGONIST; UNCLASSIFIED DRUG;

ACETYLCHOLINE RELEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN SLICE; CELL LOSS; CHOLINERGIC NERVE CELL; COGNITIVE DEFECT; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ELECTRON MICROSCOPY; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; LEARNING; MEMORY; NERVE CELL STIMULATION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT;

ANIMALS; CARRIER PROTEINS; CHOLINERGIC FIBERS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTROPHYSIOLOGY; EXCITATORY AMINO ACID AGONISTS; FRONTAL LOBE; GLYCINE; HIPPOCAMPUS; IMMUNOLOGIC TECHNIQUES; MALE; MEMBRANE TRANSPORT PROTEINS; NEURONS; OSMOLAR CONCENTRATION; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; RESORCINOLS; SEPTUM OF BRAIN; SYNAPSES; TISSUE DISTRIBUTION; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2; VESICULAR TRANSPORT PROTEINS;

EID: 3142666106     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00180.2004     Document Type: Article

References (51)

1. Aiba A, Chen C, Herrup K, Rosenmund C, Stevens CF, and Tonegawa S. Reduced hippocampal long-term potentiation and context-specific deficit in associative learning in mGluR1 mutant mice. Cell 79: 365-375, 1994.
2. Alreja M and Liu W. Noradrenaline induces IPSCs rat medial septal/diagonal band neurons: involvement of septohippocampal GABAergic neurons. J Physiol 494: 201-215, 1996.
3. Alreja M, Wu M, Liu W, Atkins JB, Leranth C, and Shanabrough M. Muscarinic tone sustains impulse flow in the septohippocampal GABA but not cholinergic pathway: implications for learning and memory. J Neurosci 20: 8103-8110, 2000.
4. Arendt T, Bruckner MK, Bigl V, and Marcova L. Dendritic reorganisation in the basal forebrain under degenerative conditions and its defects in Alzheimer's disease. II. Aging, Korsakoff's disease, Parkinson's disease, and Alzheimer's disease. J Comp Neurol 351: 189-222, 1995.
5. Balschun D and Wetzel W. Inhibition of mGluR5 blocks hippocampal LTP in vivo and spatial learning in rats. Pharmacol Biochem Behav 73: 375-380, 2002.
6. Blanchard BJ, Thomas VL, and Ingram VM. Mechanism of membrane depolarization caused by the Alzheimer Abeta1-42 peptide. Biochem Biophys Res Commun 293: 1197-1203, 2002.
7. Bokor H, Csaki A, Kocsis K, and Kiss J. Cellular architecture of the nucleus reuniens thalami and its putative aspartatergic/glutamatergic projection to the hippocampus and medial septum in the rat. Eur J Neurosci 16: 1227-1239, 2002.
8. Bruno V, Battaglia G, Copani A, Cespedes VM, Galindo MF, Cena V, Sanchez-Prieto J, Gasparini F, Kuhn R, Flor PJ, and Nicoletti F. An activity-dependent switch from facilitation to inhibition in the control of excitotoxicity by group I metabotropic glutamate receptors. Eur J Neurosci 13: 1469-1478, 2001.
9. 3H]D- aspartate autoradiography. Neuroscience 101: 637-655, 2000.
10. Csaki A, Kocsis K, Kiss J, and Halasz B. Localization of putative glutamatergic/aspartatergic neurons projecting to the supraoptic nucleus area of the rat hypothalamus. Eur J Neurosci 16: 55-68, 2002.
11. Fremeau RT, Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, and Edwards RH. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31: 247-260, 2001.
12. Gee CE, Benquet P, and Gerber U. Group I metabotropic glutamate-receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol 546: 655-664, 2003.
13. Gorelova N and Reiner PB. Role of the after hyperpolarization in control of discharge properties of septal cholinergic neurons in vitro. J Neurophysiol 75: 695-706, 1996.
14. Griffith WH and Matthews RT. Electrophysiology of AChE-positive neurons in basal forebrain slices. Neurosci Lett 71: 169-174, 1986.
15. Hajszan T, Alreja M, and Leranth C. Intrinsic vesicular glutamate transporter 2-immunoreactive input to septo-hippocampal parvalbumin-containing neurons: novel glutamatergic local circuit cells. Hippocampus Online, February 2004.
16. Hajszan T and Zaborszky L. Direct catecholaminergic-cholinergic interactions in the basal forebrain. III. Adrenergic innervation of choline acetyltransferase-containing neurons in the rat. J Comp Neurol 449: 141-157, 2002.
17. Hartig W, Seeger J, Naumann T, Brauer K, and Bruckner G. Selective in vivo fluorescence labelling of cholinergic neurons containing p75(NTR) in the rat basal forebrain. Brain Res 808: 155-165, 1998.
18. Ireland DR and Abraham WC. Group I mGluRs increase excitability of hippocampal CA1 pyramidal neurons by a PLC-independent mechanism. J Neurophysiol 88: 107-116, 2002.
19. Izquierdo I. Mechanism of action of scopolamine as an amnestic. Trends Pharmacol Sci 10: 175-177, 1989.
20. Jaskiw GE, Tizabi Y, Lipska BK, Kolachana BS, Wyatt RJ, and Gilad GM. Evidence for a frontocortical-septal glutamatergic pathway and compensatory changes in septal glutamate uptake after cortical and fornix lesions in the rat. Brain Res 550: 7-10, 1991.
21. Kettunen P, Hess D, and El Manira A. mGluR1, but not mGluR5, mediates depolarization of spinal cord neurons by blocking a leak current. J Neurophysiol 90: 2341-2348, 2003.
22. 3H]D-aspartate labeling and immunocytochemistry. Neuroscience 111: 671-691, 2002.
23. Kopelman MD and Corn TH. Cholinergic "blockade" as a model for cholinergic depletion. A comparison of the memory deficits with those of Alzheimer-type dementia and the alcoholic Korsakoff syndrome. Brain 111: 1079-1110, 1988.
24. Lee K and Boden PR. Characterization of the inward current induced by metabotropic glutamate receptor stimulation in rat ventromedial hypothalamic neurones. J Physiol 504: 649-663, 1997.
25. Leranth C, Carpi D, Buzsaki G, and Kiss J. The entorhino-septo- supramammillary nucleus connection in the rat: morphological basis of a feedback mechanism regulating hippocampal theta rhythm. Neuroscience 88: 701-718, 1999.
26. Leranth C and Kiss J. A population of supramammillary area calretinin neurons terminating on medial septal area cholinergic and lateral septal area calbindin-containing cells are aspartate/glutamatergic. J Neurosci 16: 7699-7710, 1996.
27. Lin W, McKinney K, Liu L, Lakhlani S, and Jennes L. Distribution of vesicular glutamate transporter-2 messenger ribonucleic acid and protein in the septum-hypothalamus of the rat. Endocrinology 144: 662-670, 2003.
28. Mannaioni G, Marino MJ, Valenti O, Traynelis SF, and Conn PJ. Metabotropic glutamate receptors 1 and 5 differentially regulate CA1 pyramidal cell function. J Neurosci 21: 5925-5934, 2001.
29. Manns ID, Mainville L, and Jones BE. Evidence for glutamate, in addition to acetylcholine and GABA, neurotransmitter synthesis in basal forebrain neurons projecting to the entorhinal cortex. Neuroscience 107: 249-263, 2001.
30. Marino MJ, Wittmann M, Bradley SR, Hubert GW, Smith Y, and Conn PJ. Activation of group I metabotropic glutamate receptors produces a direct excitation and disinhibition of GABAergic projection neurons in the substantia nigra pars reticulata. J Neurosci 21: 7001-7012, 2001.
31. 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.
32. Merlin LR and Wong RK. Role of group I metabotropic glutamate receptors in the patterning of epileptiform activities in vitro. J Neurophysiol 78: 539-544, 1997.
33. Mufson EJ, Bothwell M, and Kordower JH. Loss of nerve growth factor receptor-containing neurons in Alzheimer's disease: a quantitative analysis across subregions of the basal forebrain. Exp Neurol 105: 221-232, 1989.
34. Neale SA, Garthwaite J, and Batchelor AM. Metabotropic glutamate receptor subtypes modulating neurotransmission at parallel fiber-Purkinje cell synapses in rat cerebellum. Neuropharmacology 41: 42-49, 2001.
35. Petersen S, Bomme C, Baastrup C, Kemp A, and Christoffersen GR. Differential effects of mGluR1 and mGlur5 antagonism on spatial learning in rats. Pharmacol Biochem Behav 73: 381-389, 2002.
36. Pisani A, Bonsi P, Centonze D, Bernardi G, and Calabresi P. Functional coexpression of excitatory mGluR1 and mGluR5 on striatal cholinergic interneurons. Neuropharmacology 40: 460-463, 2001.
37. Poisik OV, Mannaioni G, Traynelis S, Smith Y, and Conn PJ. Distinct functional roles of the metabotropic glutamate receptors 1 and 5 in the rat globus pallidus. J Neurosci 23: 122-130, 2003.
38. Raymond CR, Thompson VL, Tate WP, and Abraham WC. Metabotropic glutamate receptors trigger homosynaptic protein synthesis to prolong long-term potentiation. J Neurosci 20: 969-976, 2000.
39. Rodrigues SM, Bauer EP, Farb CR, Schafe GE, and LeDoux JE. The group I metabotropic glutamate receptor mGluR5 is required for fear memory formation and long-term potentiation in the lateral amygdala. J Neurosci 22: 5219-5229, 2002.
40. Schoepp DD. Unveiling the functions of presynaptic metabotropic glutamate receptors in the central nervous system. J Pharmacol Exp Ther 299: 12-20, 2001.
41. Schoepp DD, Goldsworthy J, Johnson BG, Salhoff CR, and Baker SR. 3,5-dihydroxyphenylglycine is a highly selective agonist for phosphoinositide-linked metabotropic glutamate receptors in the rat hippocampus. J Neurorochem 63: 769-772, 1994.
42. Schoepp DD, Jane DE, and Monn JA. Pharmacological agents acting at subtypes of metabotropic glutamate receptors. Neuropharmacology 38: 1431-1476, 1999.
43. Shahraki A and Stone TW. Interactions between adenosine and metabotropic glutamate receptors in the rat hippocampal slice. Br J Pharmacol 138: 1059-1068, 2003.
44. Valenti O, Conn PJ, and Marino MJ. Distinct physiological roles of the Gq-coupled metabotropic glutamate receptors co-expressed in the same neuronal populations. J Cell Physiol 191: 125-137, 2002.
45. White AM, Kylanpaa RA, Christie LA, McIntosh SJ, Irving AJ, and Platt B. Presynaptic group I metabotropic glutamate receptors modulate synaptic transmission in the rat superior colliculus via 4-AP sensitive K(+) channels. Br J Pharmacol 140: 1421-1433, 2003.
46. Whitehouse PJ, Price DL, Struble RG, Clark AW, Coyle JT, and Delon MR. Alzheimer's disease and senile dementia: loss of neurons in the basal forebrain. Science 215: 1237-1239, 1982.
47. Wu M, Hajszan T, Leranth C, and Alreja M. Nicotine recruits a local glutamatergic circuit to excite septohippocampal GABAergic neurons. Eur J Neurosci 18: 1155-1168, 2003a.
48. Wu M, Newton SS, Atkins JB, Xu C, Duman RS, and Alreja M. Acetylcholinesterase inhibitors activate septohippocampal GABAergic neurons via muscarinic but not nicotinic receptors. J Pharmacol Exp Ther 307: 535-543, 2003b.
49. Wu M, Shanabrough M, Leranth C, and Alreja M. Cholinergic excitation of septohippocampal GABA but not cholinergic neurons: implications for learning and memory. J Neurosci 20: 3900-3908, 2000.
50. Yamakawa Y and Hirano T. Contribution of mGluR1 to the basal activity of a mouse cerebellar Purkinje neuron. Neurosci Lett 277: 103-106, 1999.
51. Zheng F and Johnson SW. Dual modulation of gabaergic transmission by metabotropic glutamate receptors in rat ventral tegmental area. Neuroscience 119: 453-460, 2003.