5-HT3a Receptors Modulate Hippocampal Gamma Oscillations by Regulating Synchrony of Parvalbumin-Positive Interneurons

Cerebral Cortex

Volumn 26, Issue 2, 2016, Pages 576-585

  Huang, Ying ^a,b   Yoon, Kristopher ^a   Ko, Ho ^d   Jiao, Song ^a   Ito, Wataru ^a,c   Wu, Jian Young ^e   Yung, Wing Ho ^d   Lu, Bai ^f   Morozov, Alexei ^a,c  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b FUDAN UNIVERSITY   (China)

^c VIRGINIA TECH CARILION SCHOOL OF MEDICINE   (United States)

^d Prince of Wales Hospital   (Hong Kong)

^e GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^f Tsinghua University   (China)

Author keywords

5 HT3a receptors; CCK interneurons; Gamma oscillations; Hippocampus; PV interneurons

Indexed keywords

CHOLECYSTOKININ; PARVALBUMIN; POTASSIUM CHANNEL; SEROTONIN 3A RECEPTOR; 1 [2,3 DIHYDRO 1 (2' METHYLPHENACYL) 2 OXO 5 PHENYL 1H 1,4 BENZODIAZEPIN 3 YL] 3 (3 METHYLPHENYL)UREA; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; APAMIN; BENZODIAZEPINE DERIVATIVE; CARBACHOL; CHOLINERGIC RECEPTOR STIMULATING AGENT; HORMONE ANTAGONIST; PICROTOXIN; PICROTOXININ; SEROTONIN 3 RECEPTOR; SEROTONIN RECEPTOR AFFECTING AGENT;

AFTERHYPERPOLARIZATION; ANIMAL TISSUE; ARTICLE; BRAIN REGION; BRAIN SLICE; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; GAMMA RHYTHM; HIPPOCAMPUS; INTERNEURON; MENTAL DISEASE; MOUSE; NEUROMODULATION; NONHUMAN; OSCILLATION; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RECEPTOR UPREGULATION; REGULATORY MECHANISM; SPIKE; ANALOGS AND DERIVATIVES; ANIMAL; CYTOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; IN VITRO STUDY; METABOLISM; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; SPECTROSCOPY; TRANSGENIC MOUSE;

ANIMALS; APAMIN; BENZODIAZEPINES; CARBACHOL; CHOLINERGIC AGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-A RECEPTOR ANTAGONISTS; GAMMA RHYTHM; HIPPOCAMPUS; HORMONE ANTAGONISTS; IN VITRO TECHNIQUES; INTERNEURONS; MICE; MICE, TRANSGENIC; PARVALBUMINS; PATCH-CLAMP TECHNIQUES; PICROTOXIN; RECEPTORS, SEROTONIN, 5-HT3; SEROTONIN AGENTS; SPECTRUM ANALYSIS;

EID: 84960464660     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu209     Document Type: Article

References (73)

1. Adler LE, Cawthra EM, Donovan KA, Harris JG, Nagamoto HT, Olincy A, Waldo MC. 2005. Improved p50 auditory gating with ondansetron in medicated schizophrenia patients. AmJ Psychiatry. 162:386-388.
2. Armstrong C, Soltesz I. 2012. Basket cell dichotomy in microcircuit function. J Physiol. 590:683-694.
3. Bartos M, Vida I, Jonas P. 2007. Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nat Rev Neurosci. 8:45-56.
4. Bianchi D, Marasco A, Limongiello A, Marchetti C, Marie H, Tirozzi B, Migliore M. 2012. On the mechanisms underlying the depolarization block in the spiking dynamics of CA1 pyramidal neurons. J Comput Neurosci. 33:207-225.
5. Bond CT, Herson PS, Strassmaier T, Hammond R, Stackman R, Maylie J, Adelman JP. 2004. Small conductance Ca2+-activated K+ channel knock-out mice reveal the identity of calcium-dependent afterhyperpolarization currents. J Neurosci. 24:5301-5306.
6. Bracci E, Vreugdenhil M, Hack SP, Jefferys JG. 1999. On the synchronizing mechanisms of tetanically induced hippocampal oscillations. J Neurosci. 19(18):8104-8113.
7. Buhot MC, Martin S, Segu L. 2000. Role of serotonin in memory impairment. Ann Med. 32:210-221
8. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, Tsai LH, Moore CI. 2009. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature. 459:663-667.
9. Carr MF, Karlsson MP, Frank LM. 2012. Transient slow gamma synchrony underlies hippocampal memory replay. Neuron. 75:700-713.
10. Chameau P, van Hooft JA. 2006. Serotonin 5-HT(3) receptors in the central nervous system. Cell Tissue Res. 326:573-581.
11. Cho RY, Konecky RO, Carter CS. 2006. Impairments in frontal cortical gamma synchrony and cognitive control in schizophrenia. Proc Natl Acad Sci USA. 103:19878-19883.
12. Disterhoft JF, Oh MM. 2006. Learning, aging and intrinsic neuronal plasticity. Trends Neurosci. 29:587-599.
13. Faerber L, Drechsler S, Ladenburger S, Gschaidmeier H, Fischer W. 2007. The neuronal 5-HT3 receptor network after 20 years of research-evolving concepts in management of pain and inflammation. Eur J Pharmacol. 560:1-8.
14. Fell J, Axmacher N. 2011. The role of phase synchronization in memory processes. Nat Rev Neurosci. 12:105-118.
15. Ferezou I, Cauli B, Hill EL, Rossier J, Hamel E, Lambolez B. 2002. 5-HT3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci. 22:7389-7397.
16. Fisahn A. 2005. Kainate receptors and rhythmic activity in neuronal networks: hippocampal gamma oscillations as a tool. J Physiol. 562 (Pt 1):65-72.
17. Fisahn A, Contractor A, Traub RD, Buhl EH, Heinemann SF, McBain CJ. 2004. Distinct roles for the kainate receptor subunits GluR5 and GluR6 in kainate-induced hippocampal gamma oscillations. J Neurosci. 24(43):9658-9668.
18. Fisahn A, Pike FG, Buhl EH, Paulsen O. 1998. Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature. 394:186-189.
19. Foldy C, Lee SY, Szabadics J, Neu A, Soltesz I. 2007. Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nat Neurosci. 10:1128-1130.
20. Freund TF, Katona I. 2007. Perisomatic inhibition. Neuron. 56:33-42.
21. Fukushima T, Ohtsubo T, Tsuda M, Yanagawa Y, Hori Y. 2009. Facilitatory actions of serotonin type 3 receptors on GABAergic inhibitory synaptic transmission in the spinal superficial dorsal horn. J Neurophysiol. 102:1459-1471.
22. Gandal MJ, Edgar JC, Klook K, Siegel SJ. 2012. Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology. 62:1504-1518.
23. Gonzalez-Burgos I, Feria-Velasco A. 2008. Serotonin/dopamine interaction in memory formation. Prog Brain Res. 172:603-623.
24. Hajos N, Katona I, Naiem SS, MacKie K, Ledent C, Mody I, Freund TF. 2000. Cannabinoids inhibit hippocampal GABAergic transmission and network oscillations. Eur J Neurosci. 12:3239-3249.
25. Hajos N, Palhalmi J, Mann EO, Nemeth B, Paulsen O, Freund TF. 2004. Spike timing of distinct types of GABAergic interneuron during hippocampal gamma oscillations in vitro. J Neurosci. 24:9127-9137.
26. Kandel ER, SpencerWA. 1961. Electrophysiology of hippocampal neurons II After-potentials and repetitive firing. J Neurophysiol. 24:243-259.
27. Karson MA, Tang AH, Milner TA, Alger BE. 2009. Synaptic cross talk between perisomatic-targeting interneuron classes expressing cholecystokinin and parvalbumin in hippocampus. J Neurosci. 29:4140-4154.
28. Katona I, Sperlagh B, Sik A, Kafalvi A, Vizi ES, Mackie K, Freund TF. 1999. Presynaptically located CB1 cannabinoid receptors regulate GABA release from axon terminals of specific hippocampal interneurons. J Neurosci. 19:4544-4558.
29. Keimpema E, Straiker A, Mackie K, Harkany T, Hjerling-Leffler J. 2012. Sticking out of the crowd: the molecular identity and development of cholecystokinin-containing basket cells. J Physiol. 590:703-714.
30. Kim J, Isokawa M, Ledent C, Alger BE. 2002. Activation of muscarinic acetylcholine receptors enhances the release of endogenous cannabinoids in the hippocampus. J Neurosci. 22:10182-10191.
31. Klausberger T, Marton LF, O'Neill J, Huck JH, Dalezios Y, Fuentealba P, Suen WY, Papp E, Kaneko T, Watanabe M et al. 2005. Complementary roles of cholecystokinin-and parvalbumin-expressing GABAergic neurons in hippocampal network oscillations. J Neurosci. 25:9782-9793.
32. Klausberger T, Somogyi P. 2008. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science. 321:53-57.
33. Kocsis B, Brown RE, McCarley RW, Hajos M. 2013. Impact of ketamine on neuronal network dynamics: translational modeling of schizophrenia-relevant deficits. CNS Neurosci Ther. 19:437-447.
34. Koike K, Hashimoto K, Takai N, Shimizu E, Komatsu N, Watanabe H, Nakazato M, Okamura N, Stevens KE, Freedman R et al. 2005. Tropisetron improves deficits in auditory P50 suppression in schizophrenia. Schizophr Res. 76:67-72.
35. Lewis DA, Hashimoto T, Volk DW. 2005. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci. 6:312-324.
36. Losonczy A, Biro AA, Nusser Z. 2004. Persistently active cannabinoid receptors mute a subpopulation of hippocampal interneurons. Proc Natl Acad Sci USA. 101:1362-1367.
37. Ly S, Pishdari B, Lok LL, Hajos M, Kocsis B. 2013. Activation of 5-HT6 receptors modulates sleep-wake activity and hippocampal theta oscillation. ACS Chem Neurosci. 4(1):191-199.
38. Maeda T, Kaneko S, Satoh M. 1994. Inhibitory influence via 5-HT3 receptors on the induction of LTP in mossy fiber-CA3 system of guinea-pig hippocampal slices. Neurosci Res. 18:277-282.
39. Miquel MC, Emerit MB, Nosjean A, Simon A, Rumajogee P, Brisorgueil MJ, Doucet E, Hamon M, Verge D. 2002. Differential subcellular localization of the 5-HT3-As receptor subunit in the rat central nervous system. Eur J Neurosci. 15:449-457.
40. Morales M, Bloom FE. 1997. The 5-HT3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci. 17:3157-3167.
41. Neu A, Foldy C, Soltesz I. 2007. Postsynaptic origin of CB1-dependent tonic inhibition of GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol. 578:233-247.
42. Niesler B, Weiss B, Fischer C, Nothen MM, Propping P, Bondy B, Rietschel M, Maier W, Albus M, Franzek E et al. 2001. Serotonin receptor gene HTR3A variants in schizophrenic and bipolar affective patients. Pharmacogenetics. 11:21-27.
43. Oren I, Mann EO, Paulsen O, Hajos N. 2006. Synaptic currents in anatomically identified CA3 neurons during hippocampal gamma oscillations in vitro. J Neurosci. 26:9923-9934.
44. Phelps EA. 2006. Emotion and cognition: insights from studies of the human amygdala. Annu Rev Psychol. 57:27-53.
45. Ponomarenko AA, Knoche A, Korotkova TM, Haas HL. 2003. Aminergic control of high-frequency (approximately 200 Hz) network oscillations in the hippocampus of the behaving rat. Neurosci Lett. 348(2):101-104.
46. Popescu AT, Popa D, Pare D. 2009. Coherent gamma oscillations couple the amygdala and striatum during learning. Nat Neurosci. 12:801-807.
47. Puig MV, Watakabe A, Ushimaru M, Yamamori T, Kawaguchi Y. 2010. Serotonin modulates fast-spiking interneuron and synchronous activity in the rat prefrontal cortex through 5-HT1A and 5-HT2A receptors. J Neurosci. 30(6):2211-2222.
48. Ronde P, Nichols RA. 1998. High calcium permeability of serotonin 5-HT3 receptors on presynaptic nerve terminals from rat striatum. J Neurochem. 70:1094-1103.
49. Savic N, Pedarzani P, Sciancalepore M. 2001. Medium afterhyperpolarization and firing pattern modulation in interneurons of stratum radiatum in the CA3 hippocampal region. J Neurophysiol. 85:1986-1997
50. Sörman E, Wang D, Hajos M, Kocsis B. 2011. Control of hippocampal theta rhythm by serotonin: role of 5-HT2c receptors. Neuropharmacology. 61(3):489-494.
51. Spencer KM, Nestor PG, Perlmutter R, Niznikiewicz MA, Klump MC, Frumin M, Shenton ME, McCarley RW. 2004. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc Natl Acad Sci USA. 101:17288-17293.
52. Staubli U, Xu FB. 1995. Effects of 5-HT3 receptor antagonism on hippocampal theta rhythm, memory, and LTP induction in the freely moving rat. J Neurosci. 15:2445-2452.
53. Stocker M, Krause M, Pedarzani P. 1999. An apamin-sensitive Ca2 +-activated K+ current in hippocampal pyramidal neurons. Proc Natl Acad Sci USA. 96:4662-4667.
54. Storm JF. 1990. Potassium currents in hippocampal pyramidal cells. Prog Brain Res. 83:161-187.
55. Sudweeks SN, Hooft JA, Yakel JL. 2002. Serotonin 5-HT(3) receptors in rat CA1 hippocampal interneurons: functional and molecular characterization. J Physiol. 544:715-726.
56. Szabo GG, Holderith N, Gulyas AI, Freund TF, Hajos N. 2010. Distinct synaptic properties of perisomatic inhibitory cell types and their different modulation by cholinergic receptor activation in the CA3 region of the mouse hippocampus. Eur J Neurosci. 31:2234-2246.
57. Tallon-Baudry C, Mandon S, FreiwaldWA, Kreiter AK. 2004. Oscillatory synchrony in the monkey temporal lobe correlates with performance in a visual short-term memory task. Cereb Cortex. 14:713-720.
58. Thompson AJ, Lummis SC. 2007. The 5-HT3 receptor as a therapeutic target. Expert Opin Ther Targets. 11:527-540.
59. Thompson AJ, Sullivan NL, Lummis SC. 2006. Characterization of 5-HT3 receptor mutations identified in schizophrenic patients. J Mol Neurosci. 30:273-281.
60. Tombaugh GC, Rowe WB, Rose GM. 2005. The slow afterhyperpolarization in hippocampal CA1 neurons covaries with spatial learning ability in aged Fisher 344 rats. J Neurosci. 25:2609-2616.
61. Traub RD, Jefferys JG, Whittington MA. 1997. Simulation of gamma rhythms in networks of interneurons and pyramidal cells. J Comput Neurosci. 4:141-150.
62. Tukker JJ, Fuentealba P, Hartwich K, Somogyi P, Klausberger T. 2007. Cell type-specific tuning of hippocampal interneuron firing during gamma oscillations in vivo. J Neurosci. 27:8184-8189.
63. Turner TJ, Mokler DJ, Luebke JI. 2004. Calcium influx through presynaptic 5-HT3 receptors facilitates GABA release in the hippocampus: in vitro slice and synaptosome studies. Neuroscience. 129:703-718.
64. Uhlhaas PJ, Singer W. 2010. Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci. 11:100-113.
65. Varga V, Losonczy A, Zemelman BV, Borhegyi Z, Nyiri G, Domonkos A, Hangya B, Holderith N, Magee JC, Freund TF. 2009. Fast synaptic subcortical control of hippocampal circuits. Science. 326: 449-453.
66. Villalobos C, Shakkottai VG, Chandy KG, Michelhaugh SK, Andrade R. 2004. SKCa channels mediate the medium but not the slow calcium-activated afterhyperpolarization in cortical neurons. J Neurosci. 24:3537-3542.
67. Whittington MA, Stanford IM, Colling SB, Jefferys JG, Traub RD. 1997. Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J Physiol. 502(Pt 3):591-607.
68. Whittington MA, Traub RD. 2003. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 26:676-682.
69. Whittington MA, Traub RD, Jefferys JG. 1995. Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature. 373:612-615.
70. Wójtowicz AM, van den Boom L, Chakrabarty A, Maggio N, Haq RU, Behrens CJ, Heinemann U. 2009. Monoamines block kainate-and carbachol-induced gamma-oscillations but augment stimulusinduced gamma-oscillations in rat hippocampus in vitro. Hippocampus. 19(3):273-288.
71. Womelsdorf T, Schoffelen JM, Oostenveld R, Singer W, Desimone R, Engel AK, Fries P. 2007. Modulation of neuronal interactions through neuronal synchronization. Science. 316(5831):1609-1612.
72. Zeitz KP, Guy N, Malmberg AB, Dirajlal S, Martin WJ, Sun L, Bonhaus DW, Stucky CL, Julius D, Basbaum AI. 2002. The 5-HT3 subtype of serotonin receptor contributes to nociceptive processing via a novel subset of myelinated and unmyelinated nociceptors. J Neurosci. 22:1010-1019.
73. Zhou FM, Hablitz JJ. 1999. Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J Neurophysiol. 82: 2989-2999.