Serotonergic modulation of plasticity of the auditory cortex elicited by fear conditioning

Journal of Neuroscience

Volumn 27, Issue 18, 2007, Pages 4910-4918

  Ji, Weiqing ^a   Suga, Nobuo ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

Bat; Best frequency; Neuromodulatory systems; Reorganization; Stress; Tonotopic map

Indexed keywords

ALPHA METHYL SEROTONIN; RITANSERIN; SEROTONIN; SEROTONIN 2A RECEPTOR; SEROTONIN AGONIST; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; CONDITIONING; CONTROLLED STUDY; FEAR; LEARNING; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; SEROTONINERGIC SYSTEM;

ACOUSTIC STIMULATION; ANIMALS; AUDITORY CORTEX; CHIROPTERA; CONDITIONING (PSYCHOLOGY); FEAR; HEART RATE; NEURONAL PLASTICITY; SEROTONIN; SEROTONIN AGONISTS; SEROTONIN ANTAGONISTS;

EID: 34247894007     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5528-06.2007     Document Type: Article

References (62)

1. Aghajanian GK, Marek GJ (1997) Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology 36:589-599.
2. Aghajanian GK, Marek GJ (2000) Serotonin model of schizophrenia: emerging role of glutamate mechanisms. Brain Res Brain Res Rev 31:31302-31312.
3. Araneda R, Andrade R (1991) 5-Hydroxytryptamine2 and 5-hydroxytryptamine 1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 40:399-412.
4. Barnes JM, Barnes NM, Costall B, Naylor RJ, Tyers MB (1989) 5-HT3 receptors mediate inhibition of acetylcholine release in cortical tissue. Nature 338:762-763.
5. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152.
6. Berntson GG, Tuber DS, Ronca AE, Bachman DS (1983) The decerebrate human: associative learning. Exp Neurol 81:77-88.
7. Castilho VM, Brandao ML (2001) Conditioned antinociception and freezing using electrical stimulation of the dorsal periaqueductal gray or inferior colliculus as unconditioned stimulus are differentially regulated by 5-HT2A receptors in rats. Psychopharmacology (Berl) 155:154-162.
8. Chen A, Hough CJ, Li H (2003) Serotonin type II receptor activation facilitates synaptic plasticity via N-methyl-D-aspartate-mediated mechanism in the rat basolateral amygdala. Neuroscience 119:53-63.
9. Crespi D, Gobbi M, Mennini T (1997) 5-HT3 serotonin hetero-receptors inhibit [3H]acethylcholine release in rat cortical synaptosomes. Pharmacol Res 35:351-354.
10. Davies SJ, Hood SD, Argyropoulos SV, Morris K, Bell C, Witchel HJ, Jackson PR, Nutt DJ, Potokar JP (2006) Depleting serotonin enhances both cardiovascular and psychological stress reactivity in recovered patients with anxiety disorders. J Clin Psychopharmacol 26:414-418.
11. Dear SP, Fritz J, Haresign T, Ferragamo M, Simmons JA (1993) Tonotopic and functional organization in the auditory cortex of the big brown bat, Eptesicus fuscus. J Neurophysiol 70:1988-2009.
12. DeFelipe J, Hendry SH, Hashikawa T, Jones EG (1991) Synaptic relationships of serotonin-immunoreactive terminal baskets on GABA neurons in the cat auditory cortex. Cereb Cortex 1:117-133.
13. DiCara LV, Braun JJ, Pappas BA (1970) Classical conditioning and instrumental learning of cardiac and gastrointestinal responses following removal of neocortex in the rat. J Comp Physiol Psychol 73:208-216.
14. Dringenberg HC, Zalan RM (1999) Serotonin-dependent maintenance of spatial performance and electroencephalography activation after cholinergic blockade: effects of serotonergic receptor antagonists. Brain Res 837:242-253.
15. Dunn AJ (1988) Changes in plasma and brain tryptophan and brain serotonin and 5-hydroxyindoleacetic acid after footshock stress. Life Sci 42:1847-1853.
16. Eison AS, Eison MS (1994) Serotonergic mechanisms in anxiety. Prog Neuropsychopharmacol Biol Psychiatry 18:47-62.
17. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66-70.
18. Gao E, Suga N (2000) Experience-dependent plasticity in the auditory cortex and the inferior colliculus of bats: Role of the corticofugal system. Proc Natl Acad Sci USA 97:8081-8086.
19. Garnovskaya MN, Nebigil CG, Arthur JM (1995) Spurney RF, Raymond JR. 5-Hydroxytryptamine2A receptors expressed in rat renal mesangial cells inhibit cyclic AMP accumulation. Mol Pharmacol 48:230-237.
20. Gasbarri A, Sulli A, Pacitti C, McGaugh JL (1999) Serotonergic input to cholinergic neurons in the substantia innominata and nucleus basalis magnocellularis in the rat. Neuroscience 91:1129-1142.
21. Giovannini MG, Ceccarelli I, Molinari B, Cecchi M, Goldfarb J, Blandina P (1998) Serotonergic modulation of acetylcholine release from cortex of freely moving rats. J Pharmacol Exp Ther 285:1219-1225.
22. Glennon RA., Dukat M, Westkaemper RB (2000) Serotonin receptor subtypes and ligands. Neuropsychopharmacology: The Fourth Generation of Progress. Retrieved April 6, 2004, from http://www.acnp.org/G4/GN401000039/.
23. Gu Q (2002) Neuromodulatory transmitter systems in the cortex and their role in cortical plasticity. Neuroscience 111:815-835.
24. Harvey JA (2003) Role of the serotonin 5-HT (2A) receptor in learning. Learn Mem 10:355-362.
25. Harvey JA, Quinn JL, Liu R, Aloyo VJ, Romano AG (2004) Selective remodeling of rabbit frontal cortex: relationship between 5-HT2A receptor density and associative learning. Psychopharmacology (Berl) 172:435-442.
26. Hasuo H, Matsuoka T, Akasu T (2002) Activation of presynaptic 5-hydroxytryptamine 2A receptors facilitates excitatory synaptic transmission via protein kinase C in the dorsolateral septal nucleus. J Neurosci 22:7509-7517.
27. Hurley LM, Thompson AM, Pollak GD (2002) Serotonin in the inferior colliculus. Hear Res 168:1-11.
28. Inoue T, Koyama T, Yamashita I (1993) Effect of conditioned fear stress on serotonin metabolism in the rat brain. Pharmacol Biochem Behav 44:371-374.
29. Inoue T, Tsuchiya K, Koyama T (1994) Regional changes in dopamine and serotonin activation with various intensity of physical and psychological stress in the rat brain. Pharmacol Biochem Behav 49:911-920.
30. Irvine DR, Rajan R (1996) Injury- and use-related plasticity in the primary sensory cortex of adult mammals: possible relationship to perceptual learning. Clin Exp Pharmacol Physiol 23:939-947.
31. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
32. Jakab RL, Goldman-Rakic PS (2000) Segregation of serotonin 5-HT2A and 5-HT3 receptors in inhibitory circuits of the primate cerebral cortex. J Comp Neurol 417:337-348.
33. Ji W, Suga N (2003) Development of reorganization of the auditory cortex caused by fear conditioning: effect of atropine. J Neurophysiol 90:1904-1909.
34. Ji W, Gao E, Suga N (2001) Effect of acetylcholine and atropine on plasticity of central auditory neurons caused by conditioning in bats. J Neurophy 86:211-225.
35. Kandel ER (2000) Nerve cell and behavior. In: Principles of neural science, 4/e (Kandel ER, Schwartz JH, Jessell TM, eds), pp 25. New York: McGraw-Hill.
36. Lambe EK, Goldman-Rakic PS, Aghajanian GK (2000) Serotonin induces EPSCs preferentially in layer V pyramidal neurons of the frontal cortex in the rat. Cereb Cortex 10:974-980.
37. LeDoux JE, Sakaguchi A, Reis DJ (1984) Subcortical efferent projections of the medial geniculate nucleus mediate emotional responses conditioned to acoustic stimuli. J Neurosci 4:683-698.
38. Liang X, Arvanov VL, Wang RY (1998) Inhibition of NMDA-receptor mediated response in the rat medial prefrontal cortical pyramidal cells by the 5-HT3 receptor agonist SR 57227A and 5-HT: intracellular studies. Synapse 29:257-268.
39. Ma X, Suga N (2004) Lateral inhibition for center-surround reorganization of the frequency map of bat auditory cortex. J Neurophysiol 92:3192-3199.
40. Maletic-Savatic M, Malinow R, Svoboda K (1999) Rapid dendritic morphogenesis in CA1 hippocampal dendrites induced by synaptic activity. Science 283:1923-1927.
41. Malyszko J, Urano T, Yan D, Serizawa K, Kozima Y, Takada Y, Takada A (1994) Foot shock-induced changes in blood and brain serotonin and related substances in rats. Jpn J Physiol 44:35-47.
42. Maura G, Andrioli GC, Cavazzani P, Raiteri M (1992) 5-Hydroxytryptamine3 receptors sited on cholinergic axon terminals of human cerebral cortex mediate inhibition of acetylcholine release. J Neurochem 58:2334-2337.
43. Meneses A (1999) 5-HT system and cognition. Neurosci Biobehav Rev 23:1111-1125.
44. Marek GJ, Wright RA, Gewirtz JC, Schoepp DD (2001) A major role for thalamocortical afferents in serotonergic hallucinogen receptor function in the rat neocortex. Neuroscience 105:379-392.
45. Nair SG, Gudelsky GA (2004) Activation of 5-HT2 receptors enhances the release of acetylcholine in the prefrontal cortex and hippocampus of the rat. Synapse 53:202-207.
46. Ohl FW, Scheich H (2005) Learning-induced plasticity in animal and human auditory cortex. Curr Opin Neurobiol 15:470-477.
47. Polley DB, Steinberg EE, Merzenich MM (2006) Perceptual learning directs auditory cortical map reorganization through top-down influences. J Neurosci 26:4970-4982.
48. Puig MV, Santana N, Celada P, Mengod G, Artigas F (2004) In vivo excitation of GABA interneurons in the medial prefrontal cortex through 5-HT3 receptors. Cereb Cortex 14:1365-1375.
49. Quirion R, Richard J, Dam TV (1985) Evidence for the existence of serotonin type-2 receptors on cholinergic terminals in rat cortex. Brain Res 333:345-349.
50. Rasmusson DD (2000) The role of acetylcholine in cortical synaptic plasticity. Behav Brain Res 115:205-218.
51. Roerig B, Katz LC (1997) Modulation of intrinsic circuits by serotonin 5-HT3 receptors in developing ferret visual cortex. J Neurosci 17:8324-8338.
52. Romano AG, Quinn JL, Liu R, Dave KD, Schwab D, Alexander G, Aloyo VJ, Harvey JA (2006) Effect of serotonin depletion on 5-HT2A-mediated learning in the rabbit: evidence for constitutive activity of the 5-HT2A receptor in vivo. Psychopharmacology (Berl) 184:173-181.
53. Stark H, Scheich H (1997) Dopaminergic and serotonergic neurotransmission systems are differentially involved in auditory cortex learning: a long-term microdialysis study of metabolites. J Neurochem 68:691-697.
54. Stutzmann GE, LeDoux JE (1999) GABAergic antagonists block the inhibitory effects of serotonin in the lateral amygdala: a mechanism for modulation of sensory inputs related to fear conditioning. J Neurosci 19:RC8:1-4.
55. Suga N, Ma X (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat Rev Neurosci 4:783-794.
56. Waterhouse BD, Moises HC, Woodward DJ (1986) Interaction of serotonin with somatosensory cortical neuronal responses to afferent synaptic inputs and putative neurotransmitters. Brain Res Bull 17:507-518.
57. Weisstaub NV, Zhou M, Lira A, Lambe E, Gonzalez-Maeso J, Hornung JP, Sibille E, Underwood M, Itohara S, Dauer WT, Ansorge MS, Morelli E, Mann JJ, Toth M, Aghajanian G, Sealfon SC, Hen R, Gingrich JA (2006) Cortical 5-HT2A receptor signaling modulates anxiety-like behaviors in mice. Science 313:536-540.
58. 2A receptors in working memory. J Neurosci 22:2843-2854.
59. Xiao Z, Suga N (2002) Reorganization of the cochleotopic map in the bat's auditory system by inhibition. Proc Natl Acad Sci USA 99:15743-15748.
60. Yan J, Suga N (1999) Corticofugal amplification of facilitative auditory responses of subcortical combination-sensitive neurons in the mustached bat. J Neurophysiol 8:817-824.
61. Zhang Y, Suga N (1997) Corticofugal amplification of subcortical responses to single tone stimuli in the mustached bat. J Neurophysiol 78:3489-3492.
62. Zhou FM, Hablitz JJ (1999) Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J Neurophysiol 82:2989-2999.