title: Behavioral state regulation of dendrodendritic synaptic inhibition in the olfactory bulb.
abstract: Behavioral states regulate how information is processed in local neuronal circuits. Here, we asked whether dendrodendritic synaptic interactions in the olfactory bulb vary with brain and behavioral states. To examine the state-dependent change of the dendrodendritic synaptic transmission, we monitored changes in field potential responses in the olfactory bulb of urethane-anesthetized and freely behaving rats. In urethane-anesthetized rats, granule-to-mitral dendrodendritic synaptic inhibition was larger and longer when slow waves were present in the electroencephalogram (slow-wave state) than during the fast-wave state. The state-dependent alternating change in the granule-to-mitral inhibition was regulated by the cholinergic system. In addition, the frequency of the spontaneous oscillatory activity of local field potentials and periodic discharges of mitral cells in the olfactory bulb shifted in synchrony with shifts in the neocortical brain state. Freely behaving rats showed multilevel changes in dendrodendritic synaptic inhibition that corresponded to diverse behavioral states; the inhibition was the largest during slow-wave sleep state, and successively smaller during light sleep, awake immobility, and awake moving states. These results provide evidence that behavioral state-dependent global changes in cholinergic tone modulate dendrodendritic synaptic inhibition and the information processing mode in the olfactory bulb.
authors.affiliation: Department of Physiology, Graduate School of Medicine, The University of Tokyo, Bunkyo-ku, Tokyo 113-0033, Japan.
authors.forename: Yusuke
authors.initials: Y
authors.lastname: Tsuno
authors.forename: Hideki
authors.initials: H
authors.lastname: Kashiwadani
authors.forename: Kensaku
authors.initials: K
authors.lastname: Mori
mesh_terms: D000758:Anesthesia; D000818:Animals; D001522:Behavior, Animal; D018680:Cholinergic Antagonists / Q000494:pharmacology; D003712:Dendrites / Q000502:physiology*; D004558:Electric Stimulation / Q000379:methods; D004569:Electroencephalography / Q000379:methods; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D018756:GABA Antagonists / Q000494:pharmacology; D008297:Male; D008954:Models, Biological; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000166:cytology*; D009830:Olfactory Bulb / Q000166:cytology*; D009833:Olfactory Pathways / Q000502:physiology / Q000528:radiation effects; D010852:Picrotoxin / Q000494:pharmacology; D051381:Rats; D017208:Rats, Wistar; D012601:Scopolamine / Q000494:pharmacology; D013569:Synapses / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology; D014633:Valine / Q000031:analogs & derivatives / Q000494:pharmacology; D014851:Wakefulness
chemical_list: D018680:Cholinergic Antagonists; D018691:Excitatory Amino Acid Antagonists; D018756:GABA Antagonists; D010852:Picrotoxin; D012601:Scopolamine; D014633:Valine; C056639:2-amino-5-phosphopentanoic acid
references.citation: Proc Natl Acad Sci U S A. 1995 Apr 11;92(8):3371-5
references.pmid: 7724568
references.citation: Brain Res. 1969 Jun;14(1):157-72
references.pmid: 5783107
references.citation: J Neurosci. 2007 Aug 22;27(34):9105-14
references.pmid: 17715347
references.citation: J Neurophysiol. 2004 Jun;91(6):2532-40
references.pmid: 14960563
references.citation: J Neurophysiol. 1968 Nov;31(6):884-915
references.pmid: 5710539
references.citation: Neuron. 2006 Jan 19;49(2):271-83
references.pmid: 16423700
references.citation: J Neurosci. 2005 Apr 27;25(17):4365-9
references.pmid: 15858062
references.citation: Brain Res. 2003 Jan 10;959(2):304-11
references.pmid: 12493619
references.citation: Annu Rev Psychol. 1997;48:649-84
references.pmid: 9046571
references.citation: Prog Neurobiol. 1997 Mar;51(4):457-81
references.pmid: 9106902
references.citation: Neuron. 2008 Mar 27;57(6):905-16
references.pmid: 18367091
references.citation: J Neurosci. 1987 Oct;7(10):3016-28
references.pmid: 2822862
references.citation: Neuron. 2005 Apr 21;46(2):285-96
references.pmid: 15848806
references.citation: J Neurosci. 2000 Feb 15;20(4):1505-18
references.pmid: 10662840
references.citation: Rev Neurosci. 1995 Apr-Jun;6(2):125-41
references.pmid: 8564024
references.citation: Eur J Neurosci. 2000 Nov;12(11):3963-74
references.pmid: 11069592
references.citation: Science. 1999 Oct 22;286(5440):711-5
references.pmid: 10531048
references.citation: J Pharmacol Exp Ther. 1984 Feb;228(2):268-74
references.pmid: 6694111
references.citation: J Neurosci. 2005 Apr 6;25(14):3521-30
references.pmid: 15814782
references.citation: J Neurophysiol. 2004 Oct;92(4):2413-27
references.pmid: 15152015
references.citation: Neuron. 2000 Mar;25(3):625-33
references.pmid: 10774730
references.citation: Physiol Rev. 2006 Apr;86(2):409-33
references.pmid: 16601265
references.citation: Neuron. 1998 Apr;20(4):749-61
references.pmid: 9581766
references.citation: Brain Res. 1990 Oct 1;528(2):238-44
references.pmid: 2271924
references.citation: J Neurosci. 1998 Sep 1;18(17):6790-802
references.pmid: 9712650
references.citation: Eur J Neurosci. 2004 Mar;19(6):1668-72
references.pmid: 15066163
references.citation: J Neurosci. 1986 Jan;6(1):281-92
references.pmid: 3944622
references.citation: Neuron. 2002 Mar 28;34(1):115-26
references.pmid: 11931746
references.citation: Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7259-64
references.pmid: 17428916
references.citation: J Neurosci. 1987 Oct;7(10):3154-62
references.pmid: 3668621
references.citation: J Neurosci. 1999 Nov 1;19(21):9180-91
references.pmid: 10531421
references.citation: Neuroscience. 1989;31(3):551-70
references.pmid: 2687720
references.citation: J Physiol. 1978 Jun;279:569-88
references.pmid: 671363
references.citation: Science. 1993 Oct 29;262(5134):679-85
references.pmid: 8235588
references.citation: Physiol Rev. 1972 Oct;52(4):864-917
references.pmid: 4343762
references.citation: J Neurophysiol. 1999 Oct;82(4):1786-92
references.pmid: 10515968
references.citation: J Cell Sci. 1970 Jul;7(1):125-55
references.pmid: 5476853
references.citation: Trends Neurosci. 2002 Nov;25(11):564-70
references.pmid: 12392931
references.citation: Trends Neurosci. 1995 Aug;18(8):359-64
references.pmid: 7482799
references.citation: Nat Rev Neurosci. 2008 May;9(5):331-43
references.pmid: 18382465
references.citation: Eur J Neurosci. 1997 Jun;9(6):1153-61
references.pmid: 9215698
references.citation: J Neurophysiol. 1999 May;81(5):2243-52
references.pmid: 10322063
references.citation: Brain Res. 1976 Feb 27;103(3):487-99
references.pmid: 1252939
references.citation: J Comp Neurol. 1989 Jul 15;285(3):339-49
references.pmid: 2547851
references.citation: J Neurosci. 2007 Oct 10;27(41):10969-81
references.pmid: 17928438
references.citation: J Neurophysiol. 1992 May;67(5):1222-9
references.pmid: 1597708
references.citation: Pharmacol Ther. 2004 Jun;102(3):195-221
references.pmid: 15246246
references.citation: Trends Cogn Sci. 1999 Sep;3(9):351-359
references.pmid: 10461198
references.citation: J Neurosci. 2006 Aug 23;26(34):8857-65
references.pmid: 16928875
references.citation: Brain Res. 1971 Dec 10;35(1):137-49
references.pmid: 4332422