Muscarinic receptors modulate the intrinsic excitability of infralimbic neurons and consolidation of fear extinction

Neuropsychopharmacology

Volumn 37, Issue 9, 2012, Pages 2047-2056

  Santini, Edwin ^a   Sepulveda Orengo, Marian ^b   Porter, James T ^b  

^a NOVA SOUTHEASTERN UNIVERSITY   (United States)

^b PONCE SCHOOL OF MEDICINE   (Puerto Rico)

Author keywords

amygdale; fear conditioning; M type K+ channels; plasticity; prefrontal; PTSD

Indexed keywords

CEVIMELINE; MUSCARINIC RECEPTOR; SCOPOLAMINE;

AFTERHYPERPOLARIZATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; BRAIN NERVE CELL; ELECTROPHYSIOLOGY; FEAR; INFRALIMBIC NEURON; LIMBIC CORTEX; MALE; MEMORY CONSOLIDATION; NONHUMAN; PATCH CLAMP; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT;

ACTION POTENTIALS; ANIMALS; CHOLINERGIC AGENTS; EXTINCTION, PSYCHOLOGICAL; FEAR; LIMBIC SYSTEM; MALE; NEURONS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, MUSCARINIC;

EID: 84863987663     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.52     Document Type: Article

References (57)

1. Bang SJ, Brown TH (2009). Muscarinic receptors in perirhinal cortex control trace conditioning. J Neurosci 29: 4346-4350.
2. Barak S, Weiner I (2010). Differential role of muscarinic transmission within the entorhinal cortex and basolateral amygdala in the processing of irrelevant stimuli. Neuropsychopharmacology 35: 1073-1082.
3. Barros DM, Mello e Souza T, De David T, Choi H, Aguzzoli A, Madche C et al (2001). Simultaneous modulation of retrieval by dopaminergic D(1), beta-noradrenergic, serotonergic-1A and cholinergic muscarinic receptors in cortical structures of the rat. Behav Brain Res 124: 1-7.
4. Bechara A, Damasio H, Damasio AR, Lee GP (1999). Different contributions of the human amygdala and ventromedial prefrontal cortex to decision-making. J Neurosci 19: 5473-5481.
5. Blanchard DC, Blanchard RJ (1972). Innate and conditioned reactions to threat in rats with amygdaloid lesions. J Comp Physiol Psychol 811: 281-290.
6. Boccia MM, Blake MG, Baratti CM, McGaugh JL (2009). Involvement of the basolateral amygdala in muscarinic cholinergic modulation of extinction memory consolidation. Neurobiol Learn Mem 91: 93-97.
7. Bond CT, Maylie J, Adelman JP (1999). Small-conductance calciumactivated potassium channels. Ann NY Acad Sci 868: 370-378.
8. Carr DB, Surmeier DJ (2007). M1 muscarinic receptor modulation of Kir2 channels enhances temporal summation of excitatory synaptic potentials in prefrontal cortex pyramidal neurons. J Neurophysiol 97: 3432-3438.
9. Charney DS, Deutch A (1996). A functional neuroanatomy of anxiety and fear: implications for the pathophysiology and treatment of anxiety disorders. Crit Rev Neurobiol 10: 419-446.
10. Cox CL, Metherate R, Ashe JH (1994). Modulation of cellular excitability in neocortex: muscarinic receptor and second messengermediated actions of acetylcholine. Synapse 16: 123-136.
11. Dalley JW, Theobald DE, Bouger P, Chudasama Y, Cardinal RN, Robbins TW (2004). Cortical cholinergic function and deficits in visual attentional performance in rats following 192 IgGsaporin-induced lesions of the medial prefrontal cortex. Cereb Cortex 14: 922-932.
12. Egorov AV, Gloveli T, Muller W (1999). Muscarinic control of dendritic excitability and Ca(2+) signaling in CA1 pyramidal neurons in rat hippocampal slice. J Neurophysiol 82: 1909-1915.
13. Feenstra MG, Vogel M, Botterblom MH, Joosten RN, de Bruin JP (2001). Dopamine and noradrenaline efflux in the rat prefrontal cortex after classical aversive conditioning to an auditory cue. Eur J Neurosci 13: 1051-1054.
14. Fisher A, Brandeis R, Karton I, Pittel Z, Gurwitz D, Haring R et al (1991). (+-)-cis-2-methyl-spiro(1,3-oxathiolane-5,30) quinuclidine, an M1 selective cholinergic agonist, attenuates cognitive dysfunctions in an animal model of Alzheimer's disease. J Pharmacol Exp Ther 257: 392-403.
15. Fontanez-Nuin DE, Santini E, Quirk GJ, Porter JT (2011). Memory for fear extinction requires mGluR5-mediated activation of infralimbic neurons. Cereb Cortex 21: 727-735.
16. Gereau RWT, Conn PJ (1994). A cyclic AMP-dependent form of associative synaptic plasticity induced by coactivation of betaadrenergic receptors and metabotropic glutamate receptors in rat hippocampus. J Neurosci 14: 3310-3318.
17. Ghamari-Langroudi M, Bourque CW (2004). Muscarinic receptor modulation of slow afterhyperpolarization and phasic firing in rat supraoptic nucleus neurons. J Neurosci 24: 7718-7726.
18. Hasselmo ME, McGaughy J (2004). High acetylcholine levels set circuit dynamics for attention and encoding and low acetylcholine levels set dynamics for consolidation. Prog Brain Res 145: 207-231.
19. Hernandez CC, Zaika O, Tolstykh GP, Shapiro MS (2008). Regulation of neural KCNQ channels: signalling pathways, structural motifs and functional implications. J Physiol 586: 1811-1821.
20. Herremans AH, Hijzen TH, Welborn PF, Olivier B, Slangen JL (1996). Effects of infusion of cholinergic drugs into the prefrontal cortex area on delayed matching to position performance in the rat. Brain Res 711: 102-111.
21. Herry C, Ferraguti F, Singewald N, Letzkus JJ, Ehrlich I, Luthi A (2010). Neuronal circuits of fear extinction. Eur J Neurosci 31: 599-612.
22. Huang ZB, Wang H, Rao XR, Zhong GF, Hu WH, Sheng GQ (2010). Different effects of scopolamine on the retrieval of spatial memory and fear memory. Behav Brain Res 221: 604-609.
23. Hugues S, Garcia R, Lena I (2007). Time course of extracellular catecholamine and glutamate levels in the rat medial prefrontal cortex during and after extinction of conditioned fear. Synapse 61: 933-937.
24. Introini-Collison IB, Dalmaz C, McGaugh JL (1996). Amygdala beta-noradrenergic influences on memory storage involve cholinergic activation. Neurobiol Learn Mem 65: 57-64.
25. Izaki Y, Hori K, Nomura M (2001). Elevation of prefrontal acetylcholine is related to the extinction of learned behavior in rats. Neurosci Lett 306: 33-36.
26. Kaplan GB, Moore KA (2011). The use of cognitive enhancers in animal models of fear extinction. Pharmacol Biochem Behav 99: 217-228.
27. Krause M, Offermanns S, Stocker M, Pedarzani P (2002). Functional specificity of G alpha q and G alpha 11 in the cholinergic and glutamatergic modulation of potassium currents and excitability in hippocampal neurons. J Neurosci 22: 666-673.
28. Maruki K, Izaki Y, Akema T, Nomura M (2003). Effects of acetylcholine antagonist injection into the prefrontal cortex on the progress of lever-press extinction in rats. Neurosci Lett 351: 95-98.
29. McGaugh JL (2004). The amygdala modulates the consolidation of memories of emotionally arousing experiences. Annu Rev Neurosci 27: 1-28.
30. Milad MR, Orr SP, Lasko NB, Chang Y, Rauch SL, Pitman RK (2008). Presence and acquired origin of reduced recall for fear extinction in PTSD: results of a twin study. J Psychiatr Res 42: 515-520.
31. Milad MR, Pitman RK, Ellis CB, Gold AL, Shin LM, Lasko NB et al (2009). Neurobiological basis of failure to recall extinction memory in posttraumatic stress disorder. Biol Psychiatry 66: 1075-1082.
32. Moore SJ, Cooper DC, Spruston N (2009). Plasticity of burst firing induced by synergistic activation of metabotropic glutamate and acetylcholine receptors. Neuron 61: 287-300.
33. Mueller D, Porter JT, Quirk GJ (2008). Noradrenergic signaling in infralimbic cortex increases cell excitability and strengthens memory for fear extinction. J Neurosci 28: 369-375.
34. Pang MH, Kim NS, Kim IH, Kim H, Kim HT, Choi JS (2010). Cholinergic transmission in the dorsal hippocampus modulates trace but not delay fear conditioning. Neurobiol Learn Mem 94: 206-213.
35. Parikh V, Sarter M (2008). Cholinergic mediation of attention: contributions of phasic and tonic increases in prefrontal cholinergic activity. Ann NY Acad Sci 1129: 225-235.
36. Passani MB, Cangioli I, Baldi E, Bucherelli C, Mannaioni PF, Blandina P (2001). Histamine H3 receptor-mediated impairment of contextual fear conditioning and in-vivo inhibition of cholinergic transmission in the rat basolateral amygdala. Eur J Neurosci 14: 1522-1532.
37. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates, 2nd edn. Academic Press: San Diego.
38. Power AE, McIntyre CK, Litmanovich A, McGaugh JL (2003). Cholinergic modulation of memory in the basolateral amygdala involves activation of both m1 and m2 receptors. Behav Pharmacol 14: 207-213.
39. Quirk GJ, Mueller D (2008). Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 33: 56-72.
40. Sah P, Faber ES (2002). Channels underlying neuronal calciumactivated potassium currents. Prog Neurobiol 66: 345-353.
41. Santini E, Ge H, Ren K, Pena de Ortiz S, Quirk GJ (2004). Consolidation of fear extinction requires protein synthesis in the medial prefrontal cortex. J Neurosci 24: 5704-5710.
42. Santini E, Porter JT (2010). M-type potassium channels modulate the intrinsic excitability of infralimbic neurons and regulate fear expression and extinction. J Neurosci 30: 12379-12386.
43. Santini E, Quirk GJ, Porter JT (2008). Fear conditioning and extinction differentially modify the intrinsic excitability of infralimbic neurons. J Neurosci 28: 4028-4036.
44. Sarter M, Nelson CL, Bruno JP (2005). Cortical cholinergic transmission and cortical information processing in schizophrenia. Schizophr Bull 31: 117-138.
45. Schroeder JP, Packard MG (2004). Facilitation of memory for extinction of drug-induced conditioned reward: role of amygdala and acetylcholine. Learn Mem 11: 641-647.
46. Schurr A, Payne RS, Rigor BM (1995). Protection by MK-801 against hypoxia-, excitotoxin-, and depolarization-induced neuronal damage in vitro. Neurochem Int 26: 519-525.
47. Scroggs RS, Cardenas CG, Whittaker JA, Kitai ST (2001). Muscarine reduces calcium-dependent electrical activity in substantia nigra dopaminergic neurons. J Neurophysiol 86: 2966-2972.
48. Segal M, Fisher A (1992). AF102B, a muscarinic M1 receptor agonist, mimics some effects of acetylcholine on neurons of rat hippocampus slices. Eur J Pharmacol 220: 103-106.
49. Seol GH, Ziburkus J, Huang S, Song L, Kim IT, Takamiya K et al (2007). Neuromodulators control the polarity of spike-timingdependent synaptic plasticity. Neuron 55: 919-929.
50. Shirey JK, Brady AE, Jones PJ, Davis AA, Bridges TM, Kennedy JP et al (2009). A selective allosteric potentiator of the M1 muscarinic acetylcholine receptor increases activity of medial prefrontal cortical neurons and restores impairments in reversal learning. J Neurosci 29: 14271-14286.
51. Vazdarjanova A, McGaugh JL (1999). Basolateral amygdala is involved in modulating consolidation of memory for classical fear conditioning. J Neurosci 19: 6615-6622.
52. Wallenstein GV, Vago DR (2001). Intrahippocampal scopolamine impairs both acquisition and consolidation of contextual fear conditioning. Neurobiol Learn Mem 75: 245-252.
53. Warburton EC, Koder T, Cho K, Massey PV, Duguid G, Barker GR et al (2003). Cholinergic neurotransmission is essential for perirhinal cortical plasticity and recognition memory. Neuron 38: 987-996.
54. Watabe AM, Zaki PA, O'Dell TJ (2000). Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J Neurosci 20: 5924-5931.
55. Wess J, Eglen RM, Gautam D (2007). Muscarinic acetylcholine receptors: mutant mice provide new insights for drug development. Nat Rev Drug Discov 6: 721-733.
56. Winters BD, Saksida LM, Bussey TJ (2006). Paradoxical facilitation of object recognition memory after infusion of scopolamine into perirhinal cortex: implications for cholinergic system function. J Neurosci 26: 9520-9529.
57. Zhang L, Han D, Carlen PL (1996). Temporal specificity of muscarinic synaptic modulation of the Ca(2+)-dependent K+ current (ISAHP) in rat hippocampal neurones. J Physiol 496 (Part 2): 395-405.