Delta-opioid Receptors Mediate Unique Plasticity Onto Parvalbumin-expressing Interneurons in Area CA2 of the Hippocampus

Overview

Journal J Neurosci

Specialty Neurology

Date 2013 Sep 6

PMID 24005307

Citations 44

Authors

Rebecca A Piskorowski

Vivien Chevaleyre

Affiliations

Soon will be listed here.

Abstract

Inhibition is critical for controlling information transfer in the brain. However, the understanding of the plasticity and particular function of different interneuron subtypes is just emerging. Using acute hippocampal slices prepared from adult mice, we report that in area CA2 of the hippocampus, a powerful inhibitory transmission is acting as a gate to prevent CA3 inputs from driving CA2 neurons. Furthermore, this inhibition is highly plastic, and undergoes a long-term depression following high-frequency 10 Hz or theta-burst induction protocols. We describe a novel form of long-term depression at parvalbumin-expressing (PV+) interneuron synapses that is dependent on delta-opioid receptor (DOR) activation. Additionally, PV+ interneuron transmission is persistently depressed by DOR activation in area CA2 but only transiently depressed in area CA1. These results provide evidence for a differential temporal modulation of PV+ synapses between two adjacent cortical circuits, and highlight a new function of PV+ cells in controlling information transfer.

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References

Lee S, Simons S, Heldt S, Zhao M, Schroeder J, Vellano C . RGS14 is a natural suppressor of both synaptic plasticity in CA2 neurons and hippocampal-based learning and memory. Proc Natl Acad Sci U S A. 2010; 107(39):16994-8. PMC: 2947872. DOI: 10.1073/pnas.1005362107. View

Xie C, Lewis D . Depression of LTP in rat dentate gyrus by naloxone is reversed by GABAA blockade. Brain Res. 1995; 688(1-2):56-60. DOI: 10.1016/0006-8993(95)00510-w. View

Benes F, Kwok E, VINCENT S, Todtenkopf M . A reduction of nonpyramidal cells in sector CA2 of schizophrenics and manic depressives. Biol Psychiatry. 1998; 44(2):88-97. DOI: 10.1016/s0006-3223(98)00138-3. View

Erbs E, Faget L, Scherrer G, Kessler P, Hentsch D, Vonesch J . Distribution of delta opioid receptor-expressing neurons in the mouse hippocampus. Neuroscience. 2012; 221:203-13. PMC: 3424326. DOI: 10.1016/j.neuroscience.2012.06.023. View

Simons S, Escobedo Y, Yasuda R, Dudek S . Regional differences in hippocampal calcium handling provide a cellular mechanism for limiting plasticity. Proc Natl Acad Sci U S A. 2009; 106(33):14080-4. PMC: 2729023. DOI: 10.1073/pnas.0904775106. View

Wittner L, Huberfeld G, Clemenceau S, Eross L, Dezamis E, Entz L . The epileptic human hippocampal cornu ammonis 2 region generates spontaneous interictal-like activity in vitro. Brain. 2009; 132(Pt 11):3032-46. DOI: 10.1093/brain/awp238. View

Jutkiewicz E, Rice K, Traynor J, Woods J . Separation of the convulsions and antidepressant-like effects produced by the delta-opioid agonist SNC80 in rats. Psychopharmacology (Berl). 2005; 182(4):588-96. PMC: 1307499. DOI: 10.1007/s00213-005-0138-9. View

Mercer A, Eastlake K, Trigg H, Thomson A . Local circuitry involving parvalbumin-positive basket cells in the CA2 region of the hippocampus. Hippocampus. 2010; 22(1):43-56. DOI: 10.1002/hipo.20841. View

Chevaleyre V, Castillo P . Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron. 2003; 38(3):461-72. DOI: 10.1016/s0896-6273(03)00235-6. View

10.

Fuentealba P, Tomioka R, Dalezios Y, Marton L, Studer M, Rockland K . Rhythmically active enkephalin-expressing GABAergic cells in the CA1 area of the hippocampus project to the subiculum and preferentially innervate interneurons. J Neurosci. 2008; 28(40):10017-22. PMC: 4487740. DOI: 10.1523/JNEUROSCI.2052-08.2008. View

11.

Benes F . Evidence for altered trisynaptic circuitry in schizophrenic hippocampus. Biol Psychiatry. 1999; 46(5):589-99. DOI: 10.1016/s0006-3223(99)00136-5. View

12.

Rezai X, Faget L, Bednarek E, Schwab Y, Kieffer B, Massotte D . Mouse δ opioid receptors are located on presynaptic afferents to hippocampal pyramidal cells. Cell Mol Neurobiol. 2012; 32(4):509-16. PMC: 5590642. DOI: 10.1007/s10571-011-9791-1. View

13.

Le Merrer J, Rezai X, Scherrer G, Becker J, Kieffer B . Impaired hippocampus-dependent and facilitated striatum-dependent behaviors in mice lacking the δ opioid receptor. Neuropsychopharmacology. 2013; 38(6):1050-9. PMC: 3629400. DOI: 10.1038/npp.2013.1. View

14.

Ribak C, Seress L, Leranth C . Electron microscopic immunocytochemical study of the distribution of parvalbumin-containing neurons and axon terminals in the primate dentate gyrus and Ammon's horn. J Comp Neurol. 1993; 327(2):298-321. DOI: 10.1002/cne.903270211. View

15.

Wigstrom H, Gustafsson B . Facilitation of hippocampal long-lasting potentiation by GABA antagonists. Acta Physiol Scand. 1985; 125(1):159-72. DOI: 10.1111/j.1748-1716.1985.tb07703.x. View

16.

Chevaleyre V, Siegelbaum S . Strong CA2 pyramidal neuron synapses define a powerful disynaptic cortico-hippocampal loop. Neuron. 2010; 66(4):560-72. PMC: 2905041. DOI: 10.1016/j.neuron.2010.04.013. View

17.

Filliol D, Ghozland S, Chluba J, Martin M, Matthes H, Simonin F . Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses. Nat Genet. 2000; 25(2):195-200. DOI: 10.1038/76061. View

18.

Andrioli A, Alonso-Nanclares L, Arellano J, DeFelipe J . Quantitative analysis of parvalbumin-immunoreactive cells in the human epileptic hippocampus. Neuroscience. 2007; 149(1):131-43. DOI: 10.1016/j.neuroscience.2007.07.029. View

19.

Margolis E, Mitchell J, Hjelmstad G, Fields H . A novel opioid receptor-mediated enhancement of GABAA receptor function induced by stress in ventral tegmental area neurons. J Physiol. 2011; 589(17):4229-42. PMC: 3180580. DOI: 10.1113/jphysiol.2011.209023. View

20.

Wagner J, Etemad L, Thompson A . Opioid-mediated facilitation of long-term depression in rat hippocampus. J Pharmacol Exp Ther. 2001; 296(3):776-81. View