Opposing Roles of Dopamine Receptor D1- and D2-Expressing Neurons in the Anteromedial Olfactory Tubercle in Acquisition of Place Preference in Mice.

Koshi Murata,Masahiro Yamaguchi,Yugo Fukazawa,Tomoki Kinoshita,Kenta Kobayashi,Takatoshi Hikida,Akihiro Yamanaka,Hiroyuki Manabe

doi:10.3389/fnbeh.2019.00050

Koshi Murata, Masahiro Yamaguchi + Show 6 more

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https://doi.org/10.3389/fnbeh.2019.00050

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Olfaction induces adaptive motivated behaviors. Odors associated with food induce attractive behavior, whereas those associated with dangers induce aversive behavior. We previously reported that learned odor-induced attractive and aversive behaviors accompany activation of the olfactory tubercle (OT) in a domain- and cell type-specific manner. Odor cues associated with a sugar reward induced attractive behavior and c-fos expression in the dopamine receptor D1-expressing neurons (D1 neurons) in the anteromedial OT. In contrast, odor cues associated with electrical shock induced aversive behavior and c-fos expression in the pamine receptor D2-expressing neurons (D2 neurons) in the anteromedial OT, as well as the D1 neurons in the lateral OT. Here, we investigated whether the D1 and D2 neurons in the anteromedial OT play distinct roles in attractive or aversive behaviors, using optogenetic stimulation and real-time place preference (RTPP) tests. Mice expressing ChETA (ChR2/E123T)-enhanced yellow fluorescent protein (EYFP) in the D1 neurons in the anteromedial OT spent a longer time in the photo-stimulation side of the place preference chamber than the control mice expressing EYFP. On the other hand, upon optogenetic stimulation of the D2 neurons in the anteromedial OT, the mice spent a shorter time in the photo-stimulation side than the control mice. Local neural activation in the anteromedial OT during the RTPP tests was confirmed by c-fos mRNA expression. These results suggest that the D1 and D2 neurons in the anteromedial OT play opposing roles in attractive and aversive behaviors, respectively.

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Odor sensation elicits various motivations, which enable adaptive behavioral responses such as obtaining food rewards or avoiding potential dangers (Doty, 1986)
14.0 ± 4.3% of the enhanced yellow fluorescent protein (EYFP)(+) neurons expressed D1 mRNA, and approximately 83.1 ± 7.8% of them expressed D2 mRNA in the D2-Cre mice (n = 3 mice, Figures 2B,C). These data confirmed that these Cre transgenic mice exhibited preferential expression of Cre-dependent associated virus (AAV)-derived genes in the D1 and D2 neurons
We demonstrate that cell type-specific activation of the D1 and D2 neurons in the anteromedial olfactory tubercle (OT) elicits attractive and aversive behaviors, respectively

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Introduction

Odor sensation elicits various motivations, which enable adaptive behavioral responses such as obtaining food rewards or avoiding potential dangers (Doty, 1986). The OT is composed of three major types of neurons: medium spiny neurons, dwarf cells, and granule cells (Millhouse and Heimer, 1984; Xiong and Wesson, 2016). The dwarf cells are considered a smaller type of the medium spiny neurons, and express D1 but not D2 (Murata et al, 2015). The granule cells weakly express D1, and do not express D2 (Murata et al, 2015) In addition to these three types of neurons in the striatal component, the OT contains the ventral pallidal component and axon bundles that project from the striato-pallidal structure to other brain areas, forming the medial forebrain bundle (Heimer, 1978)

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