Administration of muscarinic antagonists induce changes in passive avoidance learning and in synaptic transmission in the CA1 area of the hippocampus

• Autorzy: Dobryakova Y.V. , Ivanova O.Y. , Merkevich V.A.
• Języki publikacji: EN

Abstrakty

EN

Muscarinic acetylcholine receptors (mAChR) are known to be related to learning and memory processes. Inactivation of mAChR by cholinergic antagonists have been shown to produce amnesia in a variety of behavioral tasks. In this study, we investigated the role of M1 and M2 AChR on passive avoidance learning and plasticity of synapses formed by Schaffer collaterals in freely moving rats. Experiments were performed using Wistar male rats. Seven days before testing, a recording electrode was lowered in the CA1 region under chloral hydrate anaesthesia to record the field excitatory postsynaptic potential (fEPSP) in response to Schaffer collateral stimulation. Selective M2 receptor antagonists methoctramine and selective M1 receptors antagonist pirenzepine were intraperitoneally injected immediately after training. The effects on memory retention were examined using passive avoidance training. We measured latency of the first entry into a dark compartment of the chamber. fEPSP amplitude and slope ratio were measured before shock presentation, 90 min after the shock, and 24 hour after the shock. Methoctramine significantly impaired behavior in the passive avoidance test but pirenzepine did not induce any changes compared to control. Our results showed that pirenzepine but not methoctramine supressed the amplitude of fEPSPs. On the other hand, intracerebroventricular methoctramine administration impaired passive avoidance learning and increased the amplitude of fEPSP.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2018
• Tom: 78
• Numer: 2
• Opis fizyczny: p.132-139,fig.,ref.

Twórcy

autor

Dobryakova Y.V.

• Neurophysiology of Learning Lab, Institute of Higher Nervous Activity and Neurophysiology Russian Academy of Science, Moscow, Russia

autor

Ivanova O.Y.

• Neurophysiology of Learning Lab, Institute of Higher Nervous Activity and Neurophysiology Russian Academy of Science, Moscow, Russia

autor

Merkevich V.A.

• Neurophysiology of Learning Lab, Institute of Higher Nervous Activity and Neurophysiology Russian Academy of Science, Moscow, Russia

Bibliografia

• Auerbach JM, Segal M (1994) A novel cholinergic induction of long-term potentiation in rat hippocampus. J Neurophysiol 72: 2034–2040.
• Auerbach JM, Segal M (1996) Muscarinic receptors mediating depression and long-term potentiation in rat hippocampus. J Physiol 492: 479–493.
• Aura J, Sirviö J, Riekkinen P Jr (1997) Methoctramine moderately improves memory but pirenzepine disrupts performance in delayed non-matching to position test. Eur J Pharmacol 333: 129–134.
• Bianchin M, Mello e Souza T, Medina JH, Izquierdo I (1999) The amygdala is involved in the modulation of long-term memory, but not in working or short-term memory. Neurobiol Learn Mem 71: 127–131.
• Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31–39.
• Carey GJ, Billard W, Binch H 3rd, Cohen-Williams M, Crosby G, Grzelak M, Guzik H, Kozlowski JA, Lowe DB, Pond AJ, Tedesco RP, Watkins RW, Coffin VL (2001) SCH 57790, a selective muscarinic M(2) receptor antagonist, releases acetylcholine and produces cognitive enhancement in laboratory animals. Eur J Pharmacol 431: 189–200.
• Cobb SR, Davies CH (2005) Cholinergic modulation of hippocampal cells and circuits. J Physiol 562: 81–88.
• Cole AE, Nicoll RA (1983) Acetylcholine mediates a slow synaptic potential in hippocampal pyramidal cells. Science 221: 1299–1301.
• Cousens GA, Beckley JT (2007) Antagonism of nucleus accumbens M(2) muscarinic receptors disrupts operant responding for sucrose under a progressive ratio reinforcement schedule. Behav Brain Res 181: 127–135.
• Dasari S, Gulledge AT (2011) M1 and M4 receptors modulate hippocampal pyramidal neurons. J Neurophysiol 105: 779–792.
• Dobryakova YV, Gurskaya O, Markevich VA (2014) Participation of muscarinic receptors in memory consolidation in passive avoidance learning. Acta Neurobiol Exp 74: 211–217.
• Dodd J, Dingledine R, Kelly JS (1981) The excitatory action of acetylcholine on hippocampal neurones of the guinea pig and rat maintained in vitro. Brain Res 207: 109–127.
• Doralp S, Leung LS (2008) Cholinergic modulation of hippocampal CA1 basal-dendritic long-term potentiation. Neurobiol Learn Mem 90: 382–388.
• Dragoi G, Harris KD, Buzsáki G (2003) Place representation within hippocampal networks is modified by long-term potentiation. Neuron 39: 843–853.
• Drever BD, Riedel G, Platt B (2011) The cholinergic system and hippocampal plasticity. Behav Brain Res 221: 505–514.
• Fernández de Sevilla D, Cabezas C, de Prada AN, Sánchez-Jiménez A, Buño W (2002) Selective muscarinic regulation of functional glutamatergic Schaffer collateral synapses in rat CA1 pyramidal neurons. J Physiol 545: 51–63.
• Flynn DD, Ferrari-DiLeo G, Levey AI, Mash DC (1995) Differential alterations in muscarinic receptor subtypes in Alzheimer’s disease: implications for cholinergic-based therapies. Life Sci 56: 869–876.
• Hayes J, Li S, Anwyl R, Rowan MJ (2008) A role for protein kinase A and protein kinase M zeta in muscarinic acetylcholine receptor-initiated persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 151: 604–612.
• Hoelscher C, Anwyl R, Rowan MJ (1997) Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. J Neurosci 17: 6470–6477.
• Izquierdo I, Medina JH (1997) Memory formation: the sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 68: 285–316.
• Izquierdo LA, Barros DM, Vianna MR, Coitinho A, de David e Silva T, Choi H, Moletta B, Medina JH, Izquierdo I (2002) Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22: 269–287.
• Kikusui T, Aoyagi A, Kaneko T (2000) Spatial working memory is independent of hippocampal CA1 long-term potentiation in rats. Behav Neurosci 114: 700–706.
• Lanzafame AA, Christopoulos A, Mitchelson F (2003) Cellular signaling mechanisms for muscarinic acetylcholine receptors. Receptors Channels 9: 241–260.
• Leaderbrand K, Chen HJ, Corcoran KA, Guedea AL, Jovasevic V, Wess J, Radulovic J (2016) Muscarinic acetylcholine receptors act in synergy to facilitate learning and memory. Learn Mem 23: 631–638.
• Li S, Cullen WK, Anwyl R, Rowan MJ (2007) Muscarinic acetylcholine receptor-dependent induction of persistent synaptic enhancement in rat hippocampus in vivo. Neuroscience 144: 754–761.
• Luo L, Chen WH, Wang M, Zhu DM, She JQ, Ruan DY (2008) Modulation of long-term potentiation by individual subtypes of muscarinic acetylcholine receptor in the rat dentate gyrus. Hippocampus 18: 989–995.
• Marchi M, Raiteri M (1989) Interaction acetylcholine-glutamate in rat hippocampus: involvement of two subtypes of M-2 muscarinic receptors. J Pharmacol Exp Ther 248: 1255–1260.
• Markevich V, Scorsa AM, Dawe GS, Stephenson JD (1997) Cholinergic facilitation and inhibition of long-term potentiation of CA1 in the urethane-anesthetized rats. Brain Research 754: 95–102.
• Markevich V, Grigoryan GA, Dawe GS, Stephenson JD (2007) Theta driving both inhibits and potentiates the effects of nicotine on dentate gyrus responses. Neurosci Behav Physiol 37: 403–409.
• Mishima K, Iwasaki K, Tsukikawa H, Matsumoto Y, Egashira N, Abe K, Egawa T, Fujiwara M (2000) The scopolamine-induced impairment of spatial cognition parallels the acetylcholine release in the ventral hippocampusin rats. Jpn J Pharmacol 84: 163–173.
• Ovsepian SV, Anwyl R, Rowan MJ (2004) Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 areathrough muscarinic receptor activation: in vivo study. Eur J Neurosci 20: 1267–1275.
• Paxinos G, Watson C (1998) The Rat Brain in Stereotaxic Coordinate. Academic Press, New York.
• Rouse ST, Edmunds SM, Yi H, Gilmor ML, Levey AI (2000) Localization of M(2) muscarinic acetylcholine receptor protein in cholinergic and non-cholinergic terminals in rat hippocampus. Neurosci Lett 284: 182–186.
• Sánchez G, Alvares Lde O, Oberholzer MV, Genro B, Quillfeldt J, da Costa JC, Cerveñansky C, Jerusalinsky D, Kornisiuk E (2009) M4 muscarinic receptors are involved in modulation of neurotransmission at synapses of Schaffer collaterals on CA1 hippocampal neurons in rats. J Neurosci Res 87: 691–700.
• Seeger T, Fedorova I, Zheng F, Miyakawa T, Koustova E, Gomeza J, Basile AS, Alzheimer C, Wess J (2004) M2 muscarinic acetylcholine receptor knock-out mice show deficits in behavioral flexibility, working memory, and hippocampal plasticity. J Neurosci 24: 10117–10127.
• Shinoe T, Matsui M, Taketo MM, Manabe T (2005) Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 25: 11194–11200.
• Tzavara ET, Bymaster FP, Felder CC, Wade M, Gomeza J, Wess J, McKinzie DL, Nomikos GG (2003) Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiatry 8: 673–679.
• Vannucchi MG, Scali C, Kopf SR, Pepeu G, Casamenti F (1997) Selective muscarinic antagonists differentially affect in vivo acetylcholine release and memory performances of young and aged rats. Neuroscience 79: 837–846.
• Volpicelli LA, Levey AI (2004) Muscarinic acetylcholine receptor subtypes in cerebral cortex and hippocampus. Prog Brain Res 145: 59–66.
• Witkin JM, Gordon RK, Chiang PK (1987) Comparison of in vitro actions with behavioral effects of antimuscarinic agents. J Pharmacol Exp Ther 242: 796–803.
• Witkin JM, Alvarado-Garcia R, Perez LA, Witkin KM (1988) Central oxotremorine antagonist properties of pirenzepine. Life Sci 42: 2467–2473.
• Worms P, Gueudet C, Pério A, Soubrié P (1989) Systemic injection of pirenzepine induces a deficit in passive avoidance learning in rats. Psychopharmacology 98: 286–288.
• Zeisel A, Muñoz-Manchado AB, Codeluppi S, Lönnerberg P, La Manno G, Juréus A, Marques S, Munguba H, He L, Betsholtz C, Rolny C, Castelo-Branco G, Hjerling-Leffler J, Linnarsson S (2015) Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347: 1138–1142.
• Zhang W, Basile AS, Gomeza J, Volpicelli LA, Levey AI, Wess J (2002) Characterization of central inhibitory muscarinic autoreceptors by the use of muscarinic acetylcholine receptor knock-out mice. J Neurosci 22: 1709–1717.

Identyfikatory

DOI

10.21307/ane‑2018‑012