Doublecortin-Expressing Neurons in Chinese Tree Shrew Forebrain Exhibit Mixed Rodent and Primate-Like Topographic Characteristics

Jia-Qi Ai; Rongcan Luo; Tian Tu; Chen Yang; Juan Jiang; Bo Zhang; Rui Bi; Ewen Tu; Yong-Gang Yao; Xiao-Xin Yan

doi:10.3389/fnana.2021.727883

Doublecortin-Expressing Neurons in Chinese Tree Shrew Forebrain Exhibit Mixed Rodent and Primate-Like Topographic Characteristics

Front Neuroanat. 2021 Sep 16:15:727883. doi: 10.3389/fnana.2021.727883. eCollection 2021.

Authors

Jia-Qi Ai¹, Rongcan Luo², Tian Tu³, Chen Yang¹, Juan Jiang¹, Bo Zhang⁴, Rui Bi², Ewen Tu⁴, Yong-Gang Yao^{2

5

6}, Xiao-Xin Yan¹

Affiliations

¹ Department of Anatomy and Neurobiology, Central South University Xiangya School of Medicine, Changsha, China.
² Key Laboratory of Animal Models and Human Disease Mechanisms of the Chinese Academy of Sciences & Yunan Province, and KIZ/CUHK Joint Laboratory of Bioresources and Molecular Research in Common Diseases, Kunming Institute of Zoology, Chinese Academy of Sciences, Kunming, China.
³ Department of Neurology, Xiangya Hospital, Central South University, Changsha, China.
⁴ Department of Neurology, Brain Hospital of Hunan Province, Changsha, China.
⁵ Kunming College of Life Science, University of Chinese Academy of Sciences, Kunming, China.
⁶ CSA Center for Excellence in Brain Science and Intelligence Technology, Chinese Academy of Sciences, Shanghai, China.

Abstract

Doublecortin (DCX) is transiently expressed in new-born neurons in the subventricular zone (SVZ) and subgranular zone (SGZ) related to adult neurogenesis in the olfactory bulb (OB) and hippocampal formation. DCX immunoreactive (DCX+) immature neurons also occur in the cerebral cortex primarily over layer II and the amygdala around the paralaminar nucleus (PLN) in various mammals, with interspecies differences pointing to phylogenic variation. The tree shrews (Tupaia belangeri) are phylogenetically closer to primates than to rodents. Little is known about DCX+ neurons in the brain of this species. In the present study, we characterized DCX immunoreactivity (IR) in the forebrain of Chinese tree shrews aged from 2 months- to 6 years-old (n = 18). DCX+ cells were present in the OB, SVZ, SGZ, the piriform cortex over layer II, and the amygdala around the PLN. The numerical densities of DCX+ neurons were reduced in all above neuroanatomical regions with age, particularly dramatic in the DG in the 5-6 years-old animals. Thus, DCX+ neurons are present in the two established neurogenic sites (SVZ and SGZ) in the Chinese tree shrew as seen in other mammals. DCX+ cortical neurons in this animal exhibit a topographic pattern comparable to that in mice and rats, while these immature neurons are also present in the amygdala, concentrating around the PLN as seen in primates and some nonprimate mammals.

Keywords: adult neurogenesis; cerebrum; immature neurons; mammalian evolution; neuroplasticity.