Expression of m1-m4 muscarinic acetylcholine receptor immunoreactivity in septohippocampal neurons and other identified hippocampal afferents

Journal of Comparative Neurology

Volumn 375, Issue 3, 1996, Pages 406-416

  Rouse, Susan T ^a   Levey, Allan I ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

dentate gyrus; hippocampal associational pathway; hippocampal commissural pathway; perforant pathway; retrograde tracer

Indexed keywords

MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR; MUSCARINIC M3 RECEPTOR; MUSCARINIC M4 RECEPTOR;

ANIMAL TISSUE; ARTICLE; CHOLINERGIC NERVE; DENTATE GYRUS; HIPPOCAMPUS; IMMUNOREACTIVITY; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE;

AFFERENT PATHWAYS; ANIMALS; BRAIN MAPPING; CELL COUNT; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MUSCARINIC; SEPTUM PELLUCIDUM;

EID: 0029854670     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19961118)375:3<406::AID-CNE5>3.0.CO;2-6     Document Type: Article

References (65)

1. Akasu, T., H. Hasuo, and P. Gallagher (1995) Muscarinic receptors mediating inward and outward currents in rat dorsolateral septal neurons. Soc. Neurosci. Abstr. 21:2038.
2. Amaral, D.G., and J. Kurz (1985) An analysis of the origins of the cholinergic and noncholinergic septal projections to the hippocampal formation of the rat. J. Comp. Neurol. 240:37-59.
3. Bartus, R.T., R.L.I. Dean, B. Beer, and A.S. Lippa (1982) The cholinergic hypothesis of geriatric memory dysfunction. Science 217:408-417.
4. Blitzer, R.D., O. Gil, and E.M. Landau (1990) Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci. Lett. 119:207-210.
5. Bonner, T.I., N.J. Buckley, A.C. Young, and M.R. Brann (1987) Identification of a family of muscarinic acetylcholine receptor genes. Science 237:527-532.
6. Buckley, N.J., T.I. Bonner, and M.R. Brann (1988) Localization of a family of muscarinic receptor mRNAs in rat brain. J. Neurosci. 5:4646-4652.
7. Buckley, N.J., T.I. Bonner, C.M. Buckley, and M.R. Brann (1989) Antagonist binding properties of five cloned muscarinic receptors expressed in CHO-K1 cells. Mol. Pharmacol. 35:469-476.
8. Burgard, E.C., and J.M. Sarvey (1990) Muscarinic receptor activation facilitates the induction of long-term potentiation (LTP) in the rat dentate gyrus. Neurosci. Lett. 116:34-39.
9. Bymaster, F.P., I. Heath, J.C. Hendrix, and H.E. Shannon (1993) Comparative behavioral and neurochemical activities of cholinergic antagonists in rats. J. Pharmacol. Exp. Ther. 267:16-24.
10. Callahan, M.J., J.J. Kinsora, R.E. Harbaugh, T.M. Reeder, and R.E. Davis (1993) Continuous ICV infusion of scopolamine impairs sustained attention of rhesus monkeys. Neurobiol. Aging 14:147-151.
11. Coggeshall, R.E., and H.A. Lekan (1996) Methods for determining numbers of cells and synapses: A case for more uniform standards of review. J. Comp. Neurol. 364:6-15.
12. Coyle, J.T., D.L. Price, and M.R. DeLong (1983) Alzheimer's disease: A disorder of cortical cholinergic innervation. Science 219:1184-1190.
13. Dekker, A.J.A.M., D.J. Connor, and L.J. Thal (1991) The role of cholinergic projections from the nucleus basalis in memory. Neurosci. Biobehav. Rev. 15:299-317.
14. DeVito, J.L. (1980) Subcortical projections to the hippocampal formation in squirrel monkey. Brain Res. Bull. 5:285-289.
15. Dorje, F., J. Wess, G. Lambrecht, R. Tacke, E. Mutschler, and M.R. Brann (1991) Antagonist binding profiles of five cloned human muscarinic receptor subtypes. J. Pharmacol. Exp. Ther. 256:727-733.
16. Drachman, D.A., and J.L. Leavitt (1974) Human memory and the cholinergic system. A relationship to aging? Arch. Neurol. 30:113-121.
17. Dutar, P., and R.A. Nicoll (1988) Classification of muscarinic responses in hippocampus in terms of receptor subtypes and second-messenger responses: Electrophysiological studies in vitro. J. Neurosci. 8:4214-4224.
18. Fibiger, H.C. (1991) Cholinergic mechanisms in learning, memory, and dementia: A review of recent evidence. Trends Neurosci. 14:220-223.
19. Foster, T.C., and S.A. Deadwyler (1992) Acetylcholine modulates averaged sensory evoked responses and perforant path evoked field potentials in the rat dentate gyrus. Brain Res. 587:95-101.
20. Hallanger, A.E., and B.H. Wainer (1988) Ascending projections from the pedunculopontine tegmental nucleus and the adjacent mesopontine tegmentum in the rat. J. Comp. Neurol. 274:483-515.
21. Hersch, S.M., C.A. Gutekunst, H.D. Rees, C.J. Heilman, and A.I. Levey (1994) Distribution of m1-m4 muscarinic receptor proteins in the rat striatum: Light and electron microscopic immunocytochemistry using subtype-specific antibodies. J. Neurosci. 14:3351-3363.
22. Kahle, J.S., and C.W. Cotman (1989) Carbachol depresses synaptic responses in the medial but not the lateral perforant path. Brain Res. 482:159-163.
23. Klink, R., and A. Alonso (1993) Ionic mechanisms for the subthreshold oscillations and differential electroresponsiveness of medial entorhinal cortex layer II neurons. J. Neurophysiol. 70:144-157.
24. Klink, R., and A. Alonso (1994) Ionic mechanisms of cholinergic excitation in entorhinal cortex layer II neurons. Soc. Neurosci. Abstr. 20:477.
25. Lamour, Y., M.C. Senut, M.H. Bassant, and P. Dutar (1990) Functional properties of septo-hippocampal neurons. In M. Steriade and D. Biesold (eds): Brain Cholinergic Systems. New York: Oxford University Press, pp. 265-281.
26. Leranth, C., and M. Frotscher (1987) Cholinergic innervation of hippocampal GAD- and somatostatin-immunoreactive commissural neurons. J. Comp. Neurol. 261:33-47.
27. Levey, A.I., C.A. Kitt, W.F. Simonds, D.L. Price, and M.R. Brann (1991) Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J. Neurosci. 11:3218-3226.
28. Levey, A.I., S.M. Edmunds, C.J. Heilman, T.J. Desmond, and K.A. Frey (1994) Localization of muscarinic m3 receptor protein and M3 receptor binding in rat brain. Neuroscience 63:207-221.
29. Levey, A.I., S.M. Edmunds, S.M. Hersch, R.G. Wiley, and C.J. Heilman (1995a) A light and electron microscopic study of m2 muscarinic acetylcholine receptor in the basal forebrain of the rat. J. Comp. Neurol. 351:339-356.
30. Levey, A.I., S.M. Edmunds, V. Koliatsos, R.G. Wiley, and C.J. Heilman (1995b) Expression of m1-m4 muscarinic acetylcholine receptor proteins in hippocampus and regulation by cholinergic innervation. J. Neurosci. 15:4077-4092.
31. Lynch, G., C. Gall, G. Rose, and C. Cotman (1976) Changes in the distribution of the dentate gyrus associational system following unilateral or bilateral entorhinal lesions in the adult rat. Brain Res. 110:57-71.
32. Marchi, M., and M. Raiteri (1989) Interaction acetylcholine-glutamate in rat hippocampus: Involvement of the two subtypes of M-2 muscarinic receptors. J. Pharmacol. Exp. Ther. 248:1255-1260.
33. McCormick, D.A., and D.A. Prince (1985) Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc. Natl. Acad. Sci. USA 82:6344-6348.
34. McKinney, M. (1993) Muscarinic receptor subtype-specific coupling to second messengers in neuronal systems. Progr. Brain Res. 98:333-340.
35. McKinney, M., J.H. Miller, and P.J. Aagaard (1993) Pharmacological characterization of the rat hippocampal muscarinic autoreceptor. J. Pharmacol. Exp. Ther. 264:74-78.
36. Mena, A., and A. Alonso (1994) Entorhinal cortex layer III neurons: Characterization and cholinergic excitation. Soc. Neurosci. Abstr. 20: 1527.
37. Mesulam, M.-M., L. Volicer, J.K. Marquis, E.J. Mufson, and R.C. Green (1986) Systematic regional differences in the cholinergic innervation of the primate cerebral cortex: Distribution of enzyme activities and some behavioral implications. Ann. Neurol. 19:144-151.
38. Nadler, J.V., K.W. Vaca, W.F. White, G.S. Lynch, and C.W. Cotman (1976) Aspartate and glutamate as possible transmitters of excitatory hippocampal afferents. Nature 260:538-540.
39. Nakamura, S., Y. Tani, Y. Maezono, T. Ishihara, and T. Ohno (1992) Learning deficits after unilateral AF64A lesions in the rat basal forebrain: Role of cholinergic and noncholinergic systems. Pharmacol. Biochem. Behav. 42:119-130.
40. Nilsson, O.G., G. Leanza, C. Rosenblad, D.A. Lappi, R.G. Wiley, and A. Bjorklund (1992) Spatial learning impairments in rats with selective immunolesion of the forebrain cholinergic system. Neuroreport 3:1005-1008.
41. Pang, K., M.J. Williams, and D.S. Olton (1993) Activation of the medial septal area attenuates LTP of the lateral perforant path and enhances heterosynaptic LTD of the medial perforant path in aged rats. Brain Res. 632:150-160.
42. Pasquier, D.A., and F. Reinoso-Suarez (1976) Direct projections from hypothalamus to hippocampus in the rat demonstrated by retrograde transport of horseradish peroxidase. Brain Res. 108:165-169.
43. Pasquier, D.A., and F. Reinoso-Suarez (1977) Differential efferent connections of the brainstem to the hippocampus of the cat. Brain Res. 120:540-548.
44. Paxinos, G., and C. Watson (1986) The rat brain in stereotaxic coordinates. 2nd edition. San Diego: Academic Press.
45. 3H]acetylcholine release from rat hippocampal slices. J. Pharmacol. Exp. Ther. 244:213-217.
46. Raiteri, M., R. Leardi, and M. Marchi (1984) Heterogeneity of presynaptic muscarinic receptors regulating neurotransmitter release in the rat brain. J. Pharmacol. Exp. Ther. 228:209-214.
47. Raiteri, M., M. Marchi, A. Costi, and G. Volpe (1990) Endogenous aspartate release in the rat hippocampus is inhibited by M2 "cardiac" muscarinic receptors. Eur. J. Pharmacol. 177:181-187.
48. Ribak, C.E., L. Seress, and D.G. Amaral (1985) The development, ultrastructure and synaptic connections of the mossy cells of the dentate gyrus. J. Neurocytol. 14:835-857.
49. Riley, J.N., and R.Y. Moore (1981) Diencephalic and brainstem afferents to the hippocampal formation of the rat. Brain Res. Bull. 6:437-441.
50. Rye, D.B., C.B. Saper, and B.H. Wainer (1984) Stabilization of the tetramethylbenzidine (TMB) reaction product: Application for retrograde and anterograde tracing, and combination with immunohistochemistry. J. Histochem. Cytochem. 32:1145-1153.
51. Shannon, H.E., K.G. Bemis, J.C. Hendrix, and J.S. Ward (1990) Interactions between scopolamine and muscarinic cholinergic agonists or cholinesterase inhibitors on spatial alternation performance in rats. J. Pharmacol. Exp. Ther. 255:1071-1077.
52. Soriano, E., and M. Frotscher (1994) Mossy cells of the rat fascia dentata are glutamate-immunoreactive. Hippocampus 4:65-70.
53. Steward, O. (1976) Topographical organization of the projections from the entorhinal area to the hippocampal formation of the rat. J. Comp. Neurol. 167:285-314.
54. Steward, O., and S. Scoville (1976) Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169:347-370.
55. Sun, L.R., and J.B. Suszkiw (1995) Three types of atropine sensitive responses to carbachol in acutely isolated septal neurons of the rat. Soc. Neurosci. Abstr. 21:2038.
56. Vilaro, M.T., K.H. Wiederhold, J.M. Palacios, and G. Mengod (1992) Muscarinic m2 receptor mRNA expression and receptor binding in cholinergic and noncholinergic cells in the rat brain: A correlative study using in situ hybridization histochemistry and receptor autoradiography. Neuroscience 47:367-393.
57. Vilaro, M.T., G. Mengod, G. Palacios, and J.M. Palacios (1993) Receptor distribution in the human and animal hippocampus: Focus on muscarinic acetylcholine receptors. Hippocampus 3:149-156.
58. Vilaro, M.T., J.M. Palacios, and G. Mengod (1994) Multiplicity of muscarinic autoreceptor subtypes? Comparison of the distribution of cholinergic cells and cells containing mRNA for five subtypes of muscarinic receptors in the rat brain. Mol. Brain Res. 21:30-46.
59. Wainer, B.H., A.I. Levey, D.B. Rye, M.-M. Mesulam, and E.J. Mufson (1985) Cholinergic and noncholinergic septohippocampal pathways. Neurosci. Lett. 54:45-52.
60. Wall, S.J., B.B. Wolfe, and L.F. Kromer (1994) Cholinergic deafferentation of dorsal hippocampus by fimbria-fornix lesioning differentially regulates subtypes (m1-m5) of muscarinic receptors. J. Neurochem. 62:1345-1351.
61. Weinberg, R.J., and S.L. Van Eyck (1991) A teramethylbenzidine/tungstate reaction for horse radish peroxidase histochemistry. J. Histochem. Cytochem. 39:1143-1148.
62. Williams, S., and D. Johnston (1990) Muscarinic depression of synaptic transmission at the hippocampal mossy fiber synapse. J. Neurophysiol. 64:1089-1097.
63. Wyss, J.M., L.W. Swanson, and W.M. Cowan (1979) A study of subcortical afferents to the hippocampal formation in the rat. Neuroscience 4:463-476.
64. Yamamato, C., and N. Kawai (1967) Presynaptic action of acetylcholine in thin sections from the guinea pig dentate gyrus in vitro. Exp. Neurol. 19:176-187.
65. Zaborsky, L., L. Heimer, F. Eckenstein, and C. Leranth (1986) GABAergic input to cholinergic forebrain neurons: An ultrastructural study using retrograde tracing of HRP and double immunolabelling. J. Comp. Neurol. 250:282-295.