title: Circuit-dependent striatal PKA and ERK signaling underlies rapid behavioral shift in mating reaction of male mice.
abstract: The selection of reward-seeking and aversive behaviors is controlled by two distinct D1 and D2 receptor-expressing striatal medium spiny neurons, namely the direct pathway MSNs (dMSNs) and the indirect pathway MSNs (iMSNs), but the dynamic modulation of signaling cascades of dMSNs and iMSNs in behaving animals remains largely elusive. We developed an in vivo methodology to monitor Förster resonance energy transfer (FRET) of the activities of PKA and ERK in either dMSNs or iMSNs by microendoscopy in freely moving mice. PKA and ERK were coordinately but oppositely regulated between dMSNs and iMSNs by rewarding cocaine administration and aversive electric shocks. Notably, the activities of PKA and ERK rapidly shifted when male mice became active or indifferent toward female mice during mating behavior. Importantly, manipulation of PKA cascades by the Designer Receptor recapitulated active and indifferent mating behaviors, indicating a causal linkage of a dynamic activity shift of PKA and ERK between dMSNs and iMSNs in action selection.
authors.affiliation: Department of Systems Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan; Laboratory of Bioimaging and Cell Signaling and Laboratory for Memory Mechanisms, Brain Science Institute, RIKEN, Saitama 351-0198, Japan; and.
authors.forename: Akihiro
authors.initials: A
authors.lastname: Goto
authors.affiliation: Department of Systems Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan; Laboratory of Molecular Cell Biology and Development, Graduate School of Biostudies, and.
authors.forename: Ichiro
authors.initials: I
authors.lastname: Nakahara
authors.affiliation: Department of Systems Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan;
authors.forename: Takashi
authors.initials: T
authors.lastname: Yamaguchi
authors.affiliation: Department of Pathology and Biology of Diseases, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan;
authors.forename: Yuji
authors.initials: Y
authors.lastname: Kamioka
authors.affiliation: Laboratory for Mouse Genetic Engineering, Quantitative Biology Center, Cell Design Research Core, RIKEN, Hyogo 650-0047, Japan.
authors.forename: Kenta
authors.initials: K
authors.lastname: Sumiyama
authors.affiliation: Laboratory of Bioimaging and Cell Signaling and Department of Pathology and Biology of Diseases, Graduate School of Medicine, Kyoto University, Kyoto 606-8507, Japan;
authors.forename: Michiyuki
authors.initials: M
authors.lastname: Matsuda
authors.affiliation: Department of Systems Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan; funabiki@ent.kuhp.kyoto-u.ac.jp snakanis@obi.or.jp.
authors.forename: Shigetada
authors.initials: S
authors.lastname: Nakanishi
authors.affiliation: Department of Systems Biology, Osaka Bioscience Institute, Osaka 565-0874, Japan; Laboratory of Molecular Cell Biology and Development, Graduate School of Biostudies, and funabiki@ent.kuhp.kyoto-u.ac.jp snakanis@obi.or.jp.
authors.forename: Kazuo
authors.initials: K
authors.lastname: Funabiki
mesh_terms: D000818:Animals; D003042:Cocaine / Q000008:administration & dosage; D003342:Corpus Striatum / Q000502:physiology*; D017868:Cyclic AMP-Dependent Protein Kinases / Q000378:metabolism*; D004597:Electroshock; D005260:Female; D031541:Fluorescence Resonance Energy Transfer / Q000295:instrumentation / Q000379:methods; D020935:MAP Kinase Signaling System; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D017447:Receptors, Dopamine D1 / Q000502:physiology; D017448:Receptors, Dopamine D2 / Q000502:physiology; D012201:Reward; D012726:Sexual Behavior, Animal / Q000502:physiology*
chemical_list: D017447:Receptors, Dopamine D1; D017448:Receptors, Dopamine D2; D017868:Cyclic AMP-Dependent Protein Kinases; D003042:Cocaine
keywords: action selection; dorsal striatum; in vivo FRET imaging; mating behavior; microendoscope