title: Afferent-specific properties of interneuron synapses underlie selective long-term regulation of feedback inhibitory circuits in CA1 hippocampus.
abstract: Hebbian long-term potentiation (LTP) develops at specific synapses onto hippocampal CA1 oriens/alveus interneurons (OA-INs), suggesting selective regulation of distinct input pathways. Afferent-specific properties at interneuron synapses have been characterized extensively in CA3 stratum lucidum cells, but given interneuron diversity these rules of transmission and plasticity may not hold in other interneuron types. Here, we used paired recordings and demonstrate that CA2/3 pyramidal cell (PC) feedforward and CA1 PC feedback synapses onto OA-INs show distinct AMPA receptor rectification and Ca(2+) permeability, short-term plasticity and mGluR2/3-mediated inhibition. Only feedback synapses undergo Hebbian LTP. OA-IN firing during repeated synaptic stimulation displays onset-transient or late-persistent responses consistent with activation of feedforward and feedback inputs, respectively. Input-output functions are preserved after theta-burst stimulation, but late-persistent responses selectively show mGluR1-dependent long-term increases. Thus, cell type- and afferent-specific rules of transmission and plasticity underlie distinct OA-IN input-output functions, providing selective long-term regulation in feedback inhibitory networks.
authors.affiliation: Groupe de Recherche sur le Système Nerveux Central, Département de Physiologie, Université de Montréal, Succ. Centre-ville, Montréal, Québec, Canada.
authors.forename: Ariane
authors.initials: A
authors.lastname: Croce
authors.forename: Joe Guillaume
authors.initials: JG
authors.lastname: Pelletier
authors.forename: Maylis
authors.initials: M
authors.lastname: Tartas
authors.forename: Jean-Claude
authors.initials: JC
authors.lastname: Lacaille
mesh_terms: D000200:Action Potentials; D000818:Animals; D056547:CA1 Region, Hippocampal / Q000166:cytology / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D056651:CA2 Region, Hippocampal / Q000502:physiology; D056654:CA3 Region, Hippocampal / Q000502:physiology; D002118:Calcium / Q000378:metabolism; D025461:Feedback, Physiological; D066298:In Vitro Techniques; D007395:Interneurons / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D017774:Long-Term Potentiation; D009433:Neural Inhibition / Q000187:drug effects; D009434:Neural Pathways / Q000502:physiology; D009473:Neuronal Plasticity / Q000187:drug effects; D009475:Neurons, Afferent / Q000187:drug effects / Q000378:metabolism / Q000502:physiology*; D018377:Neurotransmitter Agents / Q000494:pharmacology; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000378:metabolism; D018094:Receptors, Metabotropic Glutamate / Q000378:metabolism; D009435:Synaptic Transmission / Q000187:drug effects; D013997:Time Factors
chemical_list: D018377:Neurotransmitter Agents; D018091:Receptors, AMPA; D018094:Receptors, Metabotropic Glutamate; C108822:metabotropic glutamate receptor 2; C102718:metabotropic glutamate receptor 3; D002118:Calcium
references.citation: Neuron. 1997 Feb;18(2):295-305
references.pmid: 9052799
references.citation: J Neurophysiol. 2002 Oct;88(4):1634-54
references.pmid: 12364494
references.citation: Proc Natl Acad Sci U S A. 1998 Sep 29;95(20):12004-9
references.pmid: 9751780
references.citation: Science. 2007 Mar 2;315(5816):1262-6
references.pmid: 17332410
references.citation: J Physiol. 1998 Feb 15;507 ( Pt 1):201-17
references.pmid: 9490840
references.citation: Proc Natl Acad Sci U S A. 2001 Jul 31;98(16):9401-6
references.pmid: 11447296
references.citation: J Neurosci. 2007 Sep 5;27(36):9560-72
references.pmid: 17804617
references.citation: J Physiol. 1995 Jul 15;486 ( Pt 2):305-12
references.pmid: 7473198
references.citation: Science. 1998 Feb 27;279(5355):1368-70
references.pmid: 9478900
references.citation: Eur J Neurosci. 1995 Sep 1;7(9):1882-8
references.pmid: 8528462
references.citation: J Neurosci. 1987 Jul;7(7):1979-93
references.pmid: 3612227
references.citation: J Comp Neurol. 1990 May 22;295(4):580-623
references.pmid: 2358523
references.citation: Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13304-9
references.pmid: 8917586
references.citation: J Neurophysiol. 1997 Nov;78(5):2592-601
references.pmid: 9356409
references.citation: Nat Neurosci. 2006 Nov;9(11):1359-61
references.pmid: 17041594
references.citation: Nature. 1993 Jan 7;361(6407):31-9
references.pmid: 8421494
references.citation: J Neurosci. 1996 Mar 15;16(6):2034-43
references.pmid: 8604048
references.citation: J Neurosci. 2000 Nov 15;20(22):8279-89
references.pmid: 11069934
references.citation: Nature. 2004 Jun 17;429(6993):717-23
references.pmid: 15170216
references.citation: J Physiol. 2004 Feb 15;555(Pt 1):125-35
references.pmid: 14673190
references.citation: J Neurosci Methods. 1991 Apr;37(2):173-82
references.pmid: 1715499
references.citation: Nat Neurosci. 1998 Nov;1(7):572-8
references.pmid: 10196564
references.citation: Nature. 2004 Sep 23;431(7007):453-6
references.pmid: 15386013
references.citation: Neuroscience. 1990;36(2):349-59
references.pmid: 2215928
references.citation: Neuron. 2002 Jul 3;35(1):147-59
references.pmid: 12123615
references.citation: Neuron. 2005 Apr 7;46(1):89-102
references.pmid: 15820696
references.citation: Neuron. 1995 Jul;15(1):137-45
references.pmid: 7619518
references.citation: J Neurosci. 1996 Sep 1;16(17):5334-43
references.pmid: 8757246
references.citation: J Physiol. 2000 Oct 1;528 Pt 1:123-30
references.pmid: 11018111
references.citation: J Physiol. 2009 Feb 15;587(Pt 4):713-9
references.pmid: 19218620
references.citation: Science. 2008 Jul 4;321(5885):53-7
references.pmid: 18599766
references.citation: J Neurosci. 2004 Oct 6;24(40):8873-84
references.pmid: 15470154
references.citation: Nat Rev Neurosci. 2007 Sep;8(9):687-99
references.pmid: 17704811
references.citation: Neuroscience. 2008 Jan 2;151(1):28-42
references.pmid: 18035501
references.citation: J Neurophysiol. 1999 Mar;81(3):1296-307
references.pmid: 10085356
references.citation: Science. 2001 Aug 10;293(5532):1159-63
references.pmid: 11498596
references.citation: J Pharmacol Exp Ther. 1996 Aug;278(2):669-78
references.pmid: 8768718
references.citation: J Physiol. 2005 Jan 1;562(Pt 1):9-26
references.pmid: 15539390
references.citation: Eur J Neurosci. 1995 Oct 1;7(10):2170-80
references.pmid: 8542073
references.citation: Nat Rev Neurosci. 2001 Jan;2(1):11-23
references.pmid: 11253355
references.citation: Nature. 1999 Oct 7;401(6753):594-8
references.pmid: 10524627
references.citation: J Neurophysiol. 1995 Mar;73(3):1282-94
references.pmid: 7608771
references.citation: Hippocampus. 1996;6(4):347-470
references.pmid: 8915675
references.citation: Nature. 1994 Oct 20;371(6499):704-7
references.pmid: 7935816
references.citation: Brain Struct Funct. 2007 Jul;212(1):75-83
references.pmid: 17717699
references.citation: Nat Neurosci. 2005 Jul;8(7):916-24
references.pmid: 15937481