title: Mapping of Learned Odor-Induced Motivated Behaviors in the Mouse Olfactory Tubercle.
abstract: An odor induces food-seeking behaviors when humans and animals learned to associate the odor with food, whereas the same odor elicits aversive behaviors following odor-danger association learning. It is poorly understood how central olfactory circuits transform the learned odor cue information into appropriate motivated behaviors. The olfactory tubercle (OT) is an intriguing area of the olfactory cortex in that it contains medium spiny neurons as principal neurons and constitutes a part of the ventral striatum. The OT is therefore a candidate area for participation in odor-induced motivated behaviors. Here we mapped c-Fos activation of medium spiny neurons in different domains of the mouse OT following exposure to learned odor cues. Mice were trained to associate odor cues to a sugar reward or foot shock punishment to induce odor-guided approach behaviors or aversive behaviors. Regardless of odorant types, the anteromedial domain of the OT was activated by learned odor cues that induced approach behaviors, whereas the lateral domain was activated by learned odor cues that induced aversive behaviors. In each domain, a larger number of dopamine receptor D1 type neurons were activated than D2 type neurons. These results indicate that specific domains of the OT represent odor-induced distinct motivated behaviors rather than odor stimuli, and raise the possibility that neuronal type-specific activation in individual domains of the OT plays crucial roles in mediating the appropriate learned odor-induced motivated behaviors. Significance statement: Although animals learn to associate odor cues with various motivated behaviors, the underlying circuit mechanisms are poorly understood. The olfactory tubercle (OT), a subarea of the olfactory cortex, also constitutes the ventral striatum. Here, we trained mice to associate odors with either reward or punishment and mapped odor-induced c-Fos activation in the OT. Regardless of odorant types, the anteromedial domain was activated by approach behavior-inducing odors, whereas the lateral domain was activated by aversive behavior-inducing odors. In each domain, dopamine receptor D1 neurons were preferentially activated over D2 neurons. The results indicate that specific OT domains represent odor-induced distinct motivated behaviors rather than odor types, and suggest the importance of neuronal type-specific activation in individual domains in mediating appropriate behaviors.
authors.affiliation: Department of Physiology, Graduate School of Medicine, the University of Tokyo, Tokyo 113-0033, Japan, Japan Science and Technology Agency, CREST, Tokyo 113-0033, Japan, and Division of Cell Biology and Neuroscience, Faculty of Medical Sciences, University of Fukui, Fukui 910-1193, Japan.
authors.forename: Koshi
authors.initials: K
authors.lastname: Murata
authors.affiliation: Department of Physiology, Graduate School of Medicine, the University of Tokyo, Tokyo 113-0033, Japan, Japan Science and Technology Agency, CREST, Tokyo 113-0033, Japan, and.
authors.forename: Michiko
authors.initials: M
authors.lastname: Kanno
authors.affiliation: Department of Physiology, Graduate School of Medicine, the University of Tokyo, Tokyo 113-0033, Japan, Japan Science and Technology Agency, CREST, Tokyo 113-0033, Japan, and.
authors.forename: Nao
authors.initials: N
authors.lastname: Ieki
authors.affiliation: Department of Physiology, Graduate School of Medicine, the University of Tokyo, Tokyo 113-0033, Japan, Japan Science and Technology Agency, CREST, Tokyo 113-0033, Japan, and moriken@m.u-tokyo.ac.jp yamaguti@m.u-tokyo.ac.jp.
authors.forename: Kensaku
authors.identifier: http://orcid.org/0000-0001-7853-9370
authors.initials: K
authors.lastname: Mori
authors.affiliation: Department of Physiology, Graduate School of Medicine, the University of Tokyo, Tokyo 113-0033, Japan, Japan Science and Technology Agency, CREST, Tokyo 113-0033, Japan, and moriken@m.u-tokyo.ac.jp yamaguti@m.u-tokyo.ac.jp.
authors.forename: Masahiro
authors.initials: M
authors.lastname: Yamaguchi
mesh_terms: D000818:Animals; D001245:Association Learning / Q000502:physiology*; D001522:Behavior, Animal / Q000502:physiology*; D001931:Brain Mapping / Q000379:methods*; D003463:Cues; D004193:Discrimination Learning / Q000502:physiology; D007091:Image Processing, Computer-Assisted; D007150:Immunohistochemistry; D017403:In Situ Hybridization; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D009812:Odorants; D066208:Olfactory Tubercle / Q000502:physiology*; D012903:Smell / Q000502:physiology
keywords: associative learning; motivation; olfaction; olfactory tubercle