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Tyrosine hydroxylase-immunoreactive neurons in the mushroom body of the field cricket, Gryllus bimaculatus

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Abstract

The mushroom body of the insect brain participates in processing and integrating multimodal sensory information and in various forms of learning. In the field cricket, Gryllus bimaculatus, dopamine plays a crucial role in aversive memory formation. However, the morphologies of dopamine neurons projecting to the mushroom body and their potential target neurons, the Kenyon cells, have not been characterized. Golgi impregnations revealed two classes of Kenyon cells (types I and II) and five different types of extrinsic fibers in the mushroom body. Type I cells, which are further divided into two subtypes (types I core and I surface), extend their dendrites into the anterior calyx, whereas type II cells extend many bushy dendritic branches into the posterior calyx. Axons of the two classes bifurcate between the pedunculus and lobes to form the vertical, medial and γ lobes. Immunocytochemistry to tyrosine hydroxylase (TH), a rate-limiting enzyme in dopamine biosynthesis, revealed the following four distinct classes of neurons: (1) TH-SLP projecting to the distal vertical lobe; (2) TH-IP1 extending to the medial and γ lobes; (3) TH-IP2 projecting to the basal vertical lobe; and (4) a multiglomerular projection neuron invading the anterior calyx and the lateral horn (TH-MPN). We previously proposed a model in the field cricket in which the efficiency of synapses from Kenyon cells transmitting a relevant sensory stimulus to output neurons commanding an appropriate behavioral reaction can be modified by dopaminergic neurons mediating aversive signals and here, we provide putative neural substrates for the cricket’s aversive learning. These will be instrumental in understanding the principle of aversive memory formation in this model species.

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Acknowledgments

We thank Dr. Ian A. Meinertzhagen (Dalhousie University, Canada) for critically reading this manuscript. We are also grateful to Ms. Yoshimi Watanabe for technical support in Golgi impregnation. This work was supported by Grant-in-Aid for Scientific Research (No. 16H04814 and 16K18586) to MM and Grant-in-Aid for Young Scientists (B) No. 26840109 to YH.

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  1. Faculty of Science, Hokkaido University, Sapporo, Hokkaido, 060-0810, Japan

    Yoshitaka Hamanaka & Makoto Mizunami

  2. Laboratory of Animal Physiology, Graduate School of Science, Osaka City University, 3-3-138 Sugimoto-cho, Sumiyoshi-ku, Osaka, 558-8585, Japan

    Yoshitaka Hamanaka

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  1. Yoshitaka Hamanaka
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Correspondence to Yoshitaka Hamanaka.

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Hamanaka, Y., Mizunami, M. Tyrosine hydroxylase-immunoreactive neurons in the mushroom body of the field cricket, Gryllus bimaculatus. Cell Tissue Res 376, 97–111 (2019). https://doi.org/10.1007/s00441-018-2969-9

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