Cell-type-specific modulation of feedback inhibition by serotonin in the hippocampus

Journal of Neuroscience

Volumn 31, Issue 23, 2011, Pages 8464-8569

  Winterer, Jochen ^a   Vanessa Stempel, A ^a   Dugladze, Tamar ^a   Földy, Csaba ^b   Maziashvili, Nino ^a   Zivkovic, Aleksandar R ^a   Priller, Josef ^a,d   Soltesz, Ivan ^b   Gloveli, Tengis ^a   Schmitz, Dietmar ^a,c,d,e  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

^d Cluster of Excellence NeuroCure   (Germany)

^e Einstein Foundation Berlin   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ; PARVALBUMIN; SEROTONIN; SEROTONIN 1B RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION (PARAMETERS); ENZYME ACTIVATION; FEMALE; GABAERGIC TRANSMISSION; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; MALE; NEGATIVE FEEDBACK; NERVE CELL STIMULATION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; CHOLECYSTOKININ; FEEDBACK, PHYSIOLOGICAL; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; MALE; NEURAL INHIBITION; NEURAL PATHWAYS; NEURONS; PATCH-CLAMP TECHNIQUES; RAPHE NUCLEI; RATS; RATS, WISTAR; SEROTONIN; SYNAPTIC TRANSMISSION;

EID: 79958279288     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.6382-10.2011     Document Type: Article

References (36)

1. Andrade R, Nicoll RA (1987) Pharmacologically distinct actions of serotonin on single pyramidal neurones of the rat hippocampus recorded in vitro. J Physiol 394:99-124.
2. Barnes NM, Sharp T (1999) A review of central 5-HT receptors and their function. Neuropharmacology 38:1083-1152.
3. Bendels MH, Beed P, Leibold C, Schmitz D, Johenning FW (2008) A novel control software that improves the experimental workflow of scanning photostimulation experiments. J Neurosci Methods 175:44-57.
4. Best AR, Regehr WG (2008) Serotonin evokes endocannabinoid release and retrogradely suppresses excitatory synapses. J Neurosci 28:6508-6515.
5. Boeijinga PH, Boddeke HW (1996) Activation of 5-HT1B receptors suppresses low but not high frequency synaptic transmission in the rat subic-ular cortex in vitro. Brain Res 721:59-65.
6. Cobb SR, Buhl EH, Halasy K, Paulsen O, Somogyi P (1995) Synchronization of neuronal activity in hippocampus by individual GABAergic interneu-rons. Nature 378:75-78.
7. Colino A, Halliwell JV (1987) Differential modulation of three separate K-conductances in hippocampal CA1 neurons by serotonin. Nature 328:73-77.
8. Duman RS, Heninger GR, Nestler EJ (1997) Amolecular and cellular theory of depression. Arch Gen Psychiatry 54:597-606.
9. Faber DS, Korn H (1991) Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys J 60:1288-1294.
10. Fink KB, Göthert M (2007) 5-HT receptor regulation of neurotransmitter release. Pharmacol Rev 59:360-417.
11. Földy C, Lee SY, Szabadics J, Neu A, Soltesz I (2007) Cell type-specific gating of perisomatic inhibition by cholecystokinin. Nat Neurosci 10: 1128-1130.
12. Freund TF, Katona I (2007) Perisomatic inhibition. Neuron 56:33-42.
13. Freund TF, Gulyás AI, Acsády L, Görcs T, Tóth K (1990) Serotonergic control of the hippocampus via local inhibitory interneurons. Proc Natl Acad Sci U S A 87:8501-8505.
14. Glickfeld LL, Scanziani M (2006) Distinct timing in the activity of cannabinoid-sensitive and cannabinoid-insensitive basket cells. Nat Neu-rosci 9:807-815.
15. Krishnan V, Nestler EJ (2008) The molecular neurobiology of depression. Nature 455:894-902.
16. Markram H, Wang Y, Tsodyks M (1998) Differential signaling via the same axon of neocortical pyramidal neurons. Proc Natl Acad Sci U S A 95:5323-5328.
17. McBain CJ, Fisahn A (2001) Interneurons unbound. Nat Rev Neurosci 2:11-23.
18. McMahon LL, Kauer JA (1997) Hippocampal interneurons are excited via serotonin-gated ion channels. J Neurophysiol 78:2493-2502.
19. Miles R, Tóth K, Gulyás AI, Hájos N, Freund TF (1996) Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16:815-823.
20. Mlinar B, Falsini C, Corradetti R (2003) Pharmacological characterization of 5-HT(1B) receptor-mediated inhibition of local excitatory synaptic transmission in the CA1 region of rat hippocampus. Br J Pharmacol 138:71-80.
21. Neu A, Földy C, Soltesz I (2007) Postsynaptic origin of CB1-dependent tonic inhibitionof GABA release at cholecystokinin-positive basket cell to pyramidal cell synapses in the CA1 region of the rat hippocampus. J Physiol 578:233-247.
22. Pawelzik H, Hughes DI, Thomson AM (2002) Physiological and morphological diversity of immunocytochemically defined parvalbumin- and cholecystokinin-positive interneuronesinCA1ofthe adult rat hippocampus. J Comp Neurol 443:346-367.
23. Pelkey KA, McBain CJ (2007) Differential regulation at functionally divergent release sites along a common axon. Curr Opin Neurobiol 17:366-373.
24. Pouille F, Scanziani M (2001) Enforcement of temporal fidelity in pyramidal cells by somatic feed-forward inhibition. Science 293:1159-1163.
25. Ressler KJ, Nemeroff CB (2000) Roleof serotonergic and noradrenergic systems in the pathophysiology of depression and anxiety disorders. Depress Anxiety 12[Suppl 1]:2-19.
26. Reyes A, Lujan R, Rozov A, Burnashev N, Somogyi P, Sakman B (1998) Target-cell-specific facilitation and depression in neocortical circuits. Nat Neurosci 4:279-285.
27. Sari Y (2004) Serotonin1B receptors: from proteintophysiological function and behavior. Neurosci Biobehav Rev 28:565-582.
28. Schmitz D, Empson RM, Heinemann U (1995) Serotonin reduces inhibition via 5-HT1A receptors in area CA1 of rat hippocampal slices in vitro. J Neurosci 15:7217-7225.
29. Schmitz D, Gloveli T, Empson RM, Heinemann U (1999) Potent depression of stimulus evoked field potential responses in the medial entorhinal cortex by serotonin. Br J Pharmacol 128:248-254.
30. Schmitz D, Mellor J, Breustedt J, Nicoll RA (2003) Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat Neurosci 6:1058-1063.
31. Svenningsson P, Chergui K, Rachleff I, Flajolet M, Zhang X, El Yacoubi M, Vaugeois JM, Nomikos GG, Greengard P (2006) Alterations in 5-HT1B receptor function by p11 in depression-like states. Science 311:77-80.
32. Torres GE, Chaput Y, Andrade R (1995) Cyclic AMP and protein kinase A mediate 5-hydroxytryptamine type 4 receptor regulation of calcium-activated potassium current in adult hippocampal neurons. Mol Pharmacol 47:191-197.
33. Torres GE, Arfken CL, Andrade R (1996) 5-Hydroxytryptamine4 receptors reduce afterhyperpolarization in hippocampus by inhibiting calcium-induced calcium release. Mol Pharmacol 50:1316-1322.
34. Varga V, Losonczy A, Zemelman BV, Borhegyi Z, Nyiri G, Domonkos A, Hangya B, Holderith N, Magee JC, Freund TF (2009) Fast synaptic sub-cortical control of hippocampal circuits. Science 326:449-453.
35. Voigt MM, Laurie DJ, Seeburg PH, Bach A (1991) Molecular cloning and characterization of a rat brain cDNA encoding a 5-hydroxytryptamine1B receptor. EMBO J 10:4017-4023.
36. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405.