Journal of Bionic Engineering (2023) 20:2228–2239 https://doi.org/10.1007/s42235-023-00382-6

Stratum Griseum Periventriculare?mediated Fear Emotion Regulates Motor Behavior in Pigeons

Wenbo Xu1 · Long Yang2 · Zishi Wang1 · Lifang Yang2 · Han Cheng1 · Shixin Zhu1 · Zhigang Shang2 ·

Zhenlong Wang1

Shixin Zhu sxzhu@zzu.edu.cn · Zhigang Shang zhigang_shang@zzu.edu.cn · Zhenlong Wang wzl@zzu.edu.cn · Wenbo Xu x278645818@163.com · Long Yang longyang_zzu@163.com

1 School of Life Sciences, Zhengzhou University, Zhengzhou 450001, China

2 School of Electrical and Information Engineering, Zhengzhou University, Zhengzhou 450001, China

Abstract：A pigeon robot is an ideal experimental animal for research in flying animal robots. The majority of current research publications have entailed electrical stimulation of the motor nuclei to regulate movement forcibly, and although a “virtual fear” behavior model has been proposed, the structure, location, and function of the nuclei that generate fear emotions remain obscure. Previous studies have shown that the Stratum Griseum Periventriculare (SGP) of pigeons is homologous to the mammalian periaqueductal gray (PAG), which plays an essential role in mammalian fear. To reveal the role of fear mediated by the SGP in behavioral regulation, we evaluated the structure and location of the SGP by histologic identification combined with magnetic resonance imaging, and analyzed the behavior of the SGP by electrical stimulation. Finally, the function of the SGP was verified with escape testing and homing experiments in an open field. Our results showed that the SGP is located in the pigeon midbrain and divided into two subregions, the dorsal part of the stratum griseum periventriculare (SGPd) and the ventral part of the stratum griseum periventriculare (SGPv) (the ranges were AP1.5–4.75 mm, ML1.75–6.75 mm, and DV2.2–7.1 mm), and that wired and wireless electrical stimulation freezing was the dominant behavior. In the escape test, SGP electrical stimulation caused the pigeons to flee to a safe place, while in the open-field homing test, electrical stimulation of the SGP induced evasive behavior in pigeons away from their original homing route. These results confirm that the SGP plays a crucial role in fear, and that electrical stimulation of this nucleus induces corresponding fear behaviors.

Keywords ：Pigeon cyborg · Bionic robot · Fear · Freezing · Electrical stimulation