Muscarinic acetylcholine neurotransmission enhances the late-phase of long-term potentiation in the hippocampal-prefrontal cortex pathway of rats in vivo: A possible involvement of monoaminergic systems

Neuroscience

Volumn 153, Issue 4, 2008, Pages 1309-1319

  Lopes Aguiar, C ^a   Romcy Pereira, R Neves ^a   Escorsim Szawka, R ^a   Galvis Alonso, O Yineth ^b   Anselmo Franci, J Aparecida ^a   Pereira Leite, J ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b Sao Jose do Rio Preto Medical School   (Brazil)

Author keywords

acetylcholine; hippocampus; long term potentiation; monoamines; prefrontal cortex; synaptic plasticity

Indexed keywords

5 HYDROXYINDOLEACETIC ACID; DOPAMINE; MUSCARINIC RECEPTOR; PILOCARPINE; SEROTONIN;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; EVOKED RESPONSE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; IN VIVO STUDY; MALE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT;

ACETYLCHOLINE; ANALYSIS OF VARIANCE; ANIMALS; BIOGENIC MONOAMINES; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; ELECTRIC STIMULATION; ELECTROCHEMISTRY; ELECTROENCEPHALOGRAPHY; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MUSCARINIC AGONISTS; NEURAL PATHWAYS; PILOCARPINE; PREFRONTAL CORTEX; RATS; SPECTRUM ANALYSIS; SYNAPTIC TRANSMISSION; TIME FACTORS;

EID: 43949105489     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.02.040     Document Type: Article

References (86)

1. Abe K., Nakata A., Mizutani A., and Saito H. Facilitatory but nonessential role of the muscarinic cholinergic system in the generation of long-term potentiation of population spikes in the dentate gyrus in vivo. Neuropharmacology 33 (1994) 847-852
2. Ago Y., Sato M., Nakamura S., Baba A., and Matsuda T. Lack of enhanced effect of antipsychotics combined with fluvoxamine on acetylcholine release in rat prefrontal cortex. J Pharmacol Sci 102 (2006) 419-422
3. Barbas H., and Blatt G.J. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus 5 (1995) 511-533
4. Barnes C.A., Meltzer J., Houston F., Orr G., McGann K., and Wenk G.L. Chronic treatment of old rats with donepezil or galantamine: effects on memory, hippocampal plasticity and nicotinic receptors. Neuroscience 99 (2000) 17-23
5. Blitzer R.D., Gil O., and Landau E.M. Cholinergic stimulation enhances long-term potentiation in the CA1 region of rat hippocampus. Neurosci Lett 119 (1990) 207-210
6. Boyd T.E., Trepel C., and Racine R.J. Cholinergic modulation of neocortical long-term potentiation in the awake, freely moving rat. Brain Res 881 (2000) 28-36
7. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72 (1976) 248-254
8. Bramham C.R., and Srebro B. Synaptic plasticity in the hippocampus is modulated by behavioral state. Brain Res 493 (1989) 74-86
9. Caballero-Bleda M., and Witter M.P. Projections from the presubiculum and the parasubiculum to morphologically characterized entorhinal-hippocampal projection neurons in the rat. Exp Brain Res 101 (1994) 93-108
10. Carr D.B., and Surmeier D.J. M1 muscarinic receptor modulation of Kir2 channels enhances temporal summation of excitatory synaptic potentials in prefrontal cortex pyramidal neurons. J Neurophysiol 97 (2007) 3432-3438
11. 2+-dependent intracellular signaling. J Neurophysiol 97 (2007) 2448-2464
12. Cheong M.Y., Yun S.H., Mook-Jung I., Joo I., Huh K., and Jung M.W. Cholinergic modulation of synaptic physiology in deep layer entorhinal cortex of the rat. J Neurosci Res 66 (2001) 117-121
13. Chudasama Y., Dalley J.W., Nathwani F., Bouger P., and Robbins T.W. Cholinergic modulation of visual attention and working memory: dissociable effects of basal forebrain 192-IgG-saporin lesions and intraprefrontal infusions of scopolamine. Learn Mem 11 (2004) 78-86
14. Couey J.J., Meredith R.M., Spijker S., Poorthuis R.B., Smit A.B., Brussaard A.B., and Mansvelder H.D. Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54 (2007) 73-87
15. Dalley J.W., Cardinal R.N., and Robbins T.W. Prefrontal executive and cognitive functions in rodents: neural and neurochemical substrates. Neurosci Biobehav Rev 28 (2004) 771-784
16. Degenetais E., Thierry A.M., Glowinski J., and Gioanni Y. Synaptic influence of hippocampus on pyramidal cells of the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex 13 (2003) 782-792
17. Detari L., Juhasz G., and Kukorelli T. Firing properties of cat basal forebrain neurones during sleep-wakefulness cycle. Electroencephalogr Clin Neurophysiol 58 (1984) 362-368
18. Dringenberg H.C., Hamze B., Wilson A., Speechley W., and Kuo M.C. Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine. Cereb Cortex 17 (2007) 839-848
19. Dunbar G.C., and Kuchibhatla R. Cognitive enhancement in man with ispronicline, a nicotinic partial agonist. J Mol Neurosci 30 (2006) 169-172
20. Dupin N., Mailliet F., Rocher C., Kessal K., Spedding M., and Jay T.M. Common efficacy of psychotropic drugs in restoring stress-induced impairment of prefrontal plasticity. Neurotox Res 10 (2006) 193-198
21. Fanselow M.S. Contextual fear, gestalt memories, and the hippocampus. Behav Brain Res 110 (2000) 73-81
22. Ferino F., Thierry A.M., and Glowinski J. Anatomical and electrophysiological evidence for a direct projection from Ammon's horn to the medial prefrontal cortex in the rat. Exp Brain Res 65 (1987) 421-426
23. Frey S., Bergado J.A., and Frey J.U. Modulation of late phases of long-term potentiation in rat dentate gyrus by stimulation of the medial septum. Neuroscience 118 (2003) 1055-1062
24. Funahashi S., Bruce C.J., and Goldman-Rakic P.S. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol 61 (1989) 331-349
25. Fuster J.M. Unit activity in prefrontal cortex during delayed-response performance: neuronal correlates of transient memory. J Neurophysiol 36 (1973) 61-78
26. Gemperle A., and Olpe H.R. Effects of subchronic clozapine treatment on long-term potentiation in rat prefrontal cortex. Eur Neuropsychopharmacol 14 (2004) 340-346
27. Gemperle A.Y., Enz A., Pozza M.F., Luthi A., and Olpe H.R. Effects of clozapine, haloperidol and iloperidone on neurotransmission and synaptic plasticity in prefrontal cortex and their accumulation in brain tissue: an in vitro study. Neuroscience 117 (2003) 681-695
28. Giacobini E. Cholinergic receptors in human brain: effects of aging and Alzheimer disease. J Neurosci Res 27 (1990) 548-560
29. Gill T.M., Sarter M., and Givens B. Sustained visual attention performance-associated prefrontal neuronal activity: evidence for cholinergic modulation. J Neurosci 20 (2000) 4745-4757
30. Goldman-Rakic P.S. Cellular basis of working memory. Neuron 14 (1995) 477-485
31. Goldman-Rakic P.S. The prefrontal landscape: implications of functional architecture for understanding human mentation and the central executive. Philos Trans R Soc Lond B Biol Sci 351 (1996) 1445-1453
32. Goldman-Rakic P.S. The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biol Psychiatry 46 (1999) 650-661
33. Granon S., Poucet B., Thinus-Blanc C., Changeux J.P., and Vidal C. Nicotinic and muscarinic receptors in the rat prefrontal cortex: differential roles in working memory, response selection and effortful processing. Psychopharmacology (Berl) 119 (1995) 139-144
34. Groenewegen H.J., and Uylings H.B. The prefrontal cortex and the integration of sensory, limbic and autonomic information. Prog Brain Res 126 (2000) 3-28
35. Gronier B., Perry K.W., and Rasmussen K. Activation of the mesocorticolimbic dopaminergic system by stimulation of muscarinic cholinergic receptors in the ventral tegmental area. Psychopharmacology (Berl) 147 (2000) 347-355
36. Gu Q. Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111 (2002) 815-835
37. Gulledge A.T., Park S.B., Kawaguchi Y., and Stuart G.J. Heterogeneity of phasic cholinergic signaling in neocortical neurons. J Neurophysiol 97 (2007) 2215-2229
38. Gurden H., Tassin J.P., and Jay T.M. Integrity of the mesocortical dopaminergic system is necessary for complete expression of in vivo hippocampal-prefrontal cortex long-term potentiation. Neuroscience 94 (1999) 1019-1027
39. Hasselmo M.E. Neuromodulation: acetylcholine and memory consolidation. Trends Cogn Sci 3 (1999) 351-359
40. Hasselmo M.E., and Barkai E. Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J Neurosci 15 (1995) 6592-6604
41. Hasselmo M.E., and Stern C.E. Mechanisms underlying working memory for novel information. Trends Cogn Sci 10 (2006) 487-493
42. Hironaka N., Tanaka K., Izaki Y., Hori K., and Nomura M. Memory-related acetylcholine efflux from rat prefrontal cortex and hippocampus: a microdialysis study. Brain Res 901 (2001) 143-150
43. Huang C.C., Lin H.J., and Hsu K.S. Repeated cocaine administration promotes long-term potentiation induction in rat medial prefrontal cortex. Cereb Cortex 17 (2007) 1877-1888
44. Hughes R.A. Anticholinergic drugs, blood-brain-barrier and tonic immobility in chickens. Physiol Behav 29 (1982) 67-71
45. Ichikawa J., Chung Y.C., Li Z., Dai J., and Meltzer H.Y. Cholinergic modulation of basal and amphetamine-induced dopamine release in rat medial prefrontal cortex and nucleus accumbens. Brain Res 958 (2002) 176-184
46. Iga Y., Arisawa H., Ise M., Yasuda H., and Takeshita Y. Modulation of rhythmical slow activity, long-term potentiation and memory by muscarinic receptor agonists. Eur J Pharmacol 308 (1996) 13-19
47. Izaki Y., Takita M., and Nomura M. Local properties of CA1 region in hippocampo-prefrontal synaptic plasticity in rats. Neuroreport 13 (2002) 469-472
48. Jay T.M., Burette F., and Laroche S. NMDA receptor-dependent long-term potentiation in the hippocampal afferent fibre system to the prefrontal cortex in the rat. Eur J Neurosci 7 (1995) 247-250
49. Jay T.M., Burette F., and Laroche S. Plasticity of the hippocampal-prefrontal cortex synapses. J Physiol Paris 90 (1996) 361-366
50. Jay T.M., Glowinski J., and Thierry A.M. Selectivity of the hippocampal projection to the prelimbic area of the prefrontal cortex in the rat. Brain Res 505 (1989) 337-340
51. Jay T.M., Rocher C., Hotte M., Naudon L., Gurden H., and Spedding M. Plasticity at hippocampal to prefrontal cortex synapses is impaired by loss of dopamine and stress: importance for psychiatric diseases. Neurotox Res 6 (2004) 233-244
52. Jay T.M., and Witter M.P. Distribution of hippocampal CA1 and subicular efferents in the prefrontal cortex of the rat studied by means of anterograde transport of Phaseolus vulgaris-leucoagglutinin. J Comp Neurol 313 (1991) 574-586
53. Jones M.W., and Wilson M.A. Theta rhythms coordinate hippocampal-prefrontal interactions in a spatial memory task. PLoS Biol 3 (2005) e402
54. Kawashima H., Izaki Y., Grace A.A., and Takita M. Cooperativity between hippocampal-prefrontal short-term plasticity through associative long-term potentiation. Brain Res 1109 (2006) 37-44
55. Koyama Y., and Kayama Y. Mutual interactions among cholinergic, noradrenergic and serotonergic neurons studied by ionophoresis of these transmitters in rat brainstem nuclei. Neuroscience 55 (1993) 1117-1126
56. Laroche S., Jay T.M., and Thierry A.M. Long-term potentiation in the prefrontal cortex following stimulation of the hippocampal CA1/subicular region. Neurosci Lett 114 (1990) 184-190
57. Leung L.S., Shen B., Rajakumar N., and Ma J. Cholinergic activity enhances hippocampal long-term potentiation in CA1 during walking in rats. J Neurosci 23 (2003) 9297-9304
58. Lyons D.M. Stress, depression, and inherited variation in primate hippocampal and prefrontal brain development. Psychopharmacol Bull 36 (2002) 27-43
59. Maquet P., Peters J., Aerts J., Delfiore G., Degueldre C., Luxen A., and Franck G. Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383 (1996) 163-166
60. Mark G.P., Rada P.V., and Shors T.J. Inescapable stress enhances extracellular acetylcholine in the rat hippocampus and prefrontal cortex but not the nucleus accumbens or amygdala. Neuroscience 74 (1996) 767-774
61. Mayo W., Dubois B., Ploska A., Javoy-Agid F., Agid Y., Le Moal M., and Simon H. Cortical cholinergic projections from the basal forebrain of the rat, with special reference to the prefrontal cortex innervation. Neurosci Lett 47 (1984) 149-154
62. McCormick D.A., and Prince D.A. Two types of muscarinic response to acetylcholine in mammalian cortical neurons. Proc Natl Acad Sci U S A 82 (1985) 6344-6348
63. McKinney M., Coyle J.T., and Hedreen J.C. Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217 (1983) 103-121
64. Messer Jr. W.S. The utility of muscarinic agonists in the treatment of Alzheimer's disease. J Mol Neurosci 19 (2002) 187-193
65. Ohashi S., Matsumoto M., Otani H., Mori K., Togashi H., Ueno K., Kaku A., and Yoshioka M. Changes in synaptic plasticity in the rat hippocampo-medial prefrontal cortex pathway induced by repeated treatments with fluvoxamine. Brain Res 949 (2002) 131-138
66. Pakarinen E.D., and Moerschbaecher J.M. Comparison of the effects of scopolamine and methylscopolamine on the performance of a fixed-ratio discrimination in squirrel monkeys. Pharmacol Biochem Behav 44 (1993) 815-819
67. Palkovits M. Isolated removal of hypothalamic or other brain nuclei of the rat. Brain Res 59 (1973) 449-450
68. Paxinos G., and Watson C. The rat brain in stereotaxic coordinates (1998), Academic Press, New York
69. Peleg-Raibstein D., Pezze M.A., Ferger B., Zhang W.N., Murphy C.A., Feldon J., and Bast T. Activation of dopaminergic neurotransmission in the medial prefrontal cortex by N-methyl-d-aspartate stimulation of the ventral hippocampus in rats. Neuroscience 132 (2005) 219-232
70. Raedler T.J., Bymaster F.P., Tandon R., Copolov D., and Dean B. Towards a muscarinic hypothesis of schizophrenia. Mol Psychiatry 12 (2007) 232-246
71. Ragozzino M.E., and Kesner R.P. The effects of muscarinic cholinergic receptor blockade in the rat anterior cingulate and prelimbic/infralimbic cortices on spatial working memory. Neurobiol Learn Mem 69 (1998) 241-257
72. Romcy-Pereira R., and Pavlides C. Distinct modulatory effects of sleep on the maintenance of hippocampal and medial prefrontal cortex LTP. Eur J Neurosci 20 (2004) 3453-3462
73. Sarter M., and Bruno J.P. Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res Brain Res Rev 23 (1997) 28-46
74. Sarter M., Nelson C.L., and Bruno J.P. Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr Bull 31 (2005) 117-138
75. Satoh K., and Fibiger H.C. Cholinergic neurons of the laterodorsal tegmental nucleus: efferent and afferent connections. J Comp Neurol 253 (1986) 277-302
76. Scoville W.B., and Milner B. Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20 (1957) 11-21
77. Siapas A.G., Lubenov E.V., and Wilson M.A. Prefrontal phase locking to hippocampal theta oscillations. Neuron 46 (2005) 141-151
78. Squire L.R. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99 (1992) 195-231
79. Stanhope K.J., Mirza N.R., Bickerdike M.J., Bright J.L., Harrington N.R., Hesselink M.B., Kennett G.A., Lightowler S., Sheardown M.J., Syed R., Upton R.L., Wadsworth G., Weiss S.M., and Wyatt A. The muscarinic receptor agonist xanomeline has an antipsychotic-like profile in the rat. J Pharmacol Exp Ther 299 (2001) 782-792
80. Swanson L.W. A direct projection from Ammon's horn to prefrontal cortex in the rat. Brain Res 217 (1981) 150-154
81. Swanson L.W., and Cowan W.M. An autoradiographic study of the organization of the efferent connections of the hippocampal formation in the rat. J Comp Neurol 172 (1977) 49-84
82. Takita M., Izaki Y., Jay T.M., Kaneko H., and Suzuki S.S. Induction of stable long-term depression in vivo in the hippocampal-prefrontal cortex pathway. Eur J Neurosci 11 (1999) 4145-4148
83. van Haaren F., and van Hest A. The effects of scopolamine and methylscopolamine on visual and auditory discriminations in male and female Wistar rats. Pharmacol Biochem Behav 32 (1989) 707-710
84. Verdier D., and Dykes R.W. Long-term cholinergic enhancement of evoked potentials in rat hindlimb somatosensory cortex displays characteristics of long-term potentiation. Exp Brain Res 137 (2001) 71-82
85. Vertes R.P. Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142 (2006) 1-20
86. Witter M.P., and Amaral D.G. Hippocampal formation. In: Paxinos G. (Ed). The rat nervous system (2004), Elsevier Academic Press, San Diego 637-703