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The Tree Shrew (Tupaia belangeri chinensis) Brain in Stereotaxic Coordinates
Abstract
This atlas is currently the most systematic and comprehensive atlas of the tree shrew brain. The purpose of this book is to help scientists acquire accurate coordinates of the brain regions of the tree shrew, which is becoming a popular animal model for a variety of human diseases. This atlas contains series of 192 coronal sections, 36 sagittal sections, and 49 horizontal sections using Nissl staining or acetylcholinesterase histochemistry as well as a series of diagrams in stereotaxic coordinates. Original photomicrographs are obtained at single-cell resolution. In addition, we also referred to magnetic resonance images acquired at 250 um intervals with a magnetic resonance scanner 9.4T. Many brain structures are first identified in tree shrews and accurately presented in a stereotaxic coordinate system. The Bregma coordinates system is used for the first time in this tree shrew brain atlas. The atlas represents the collaboration between two indispensable skills of brain research, neuroanatomy and stereotaxic surgery. It will be extensively used in neuroscience research, particularly tree shrew brain study, and will help graduate students and researchers understand brain anatomy and acquire accurate reference coordinates.
Chapters (4)
Tree shrews belong to the order Scandentia; they are day-active animals that live in arboreal habitats in South and Southeast Asia (Peng et al. 1991). Recently, whole-genome sequencing of the Chinese tree shrew (Tupaia belangeri chinensis) was completed (Fan et al. 2013). According to recent studies, tree shrews are the closest living relatives of primates (Janecka et al. 2007; Kriegs et al. 2007; Fan et al. 2013; McCollum and Roberts 2014). The tree shrew is a good model species because they are day-active animals, they are small in size (12–18 cm and 110–180 g), they are easy to handle and feed, and they have a relatively short gestation period (41–55 days) and length of puberty (2–6 months). They are also a good choice for reasons related to ethical considerations. There have been many recent attempts to use tree shrews as an animal model. They have been used, for example, in studies of viral infections (Yan et al. 1996; Zhao et al. 2002; Tsukiyama-Kohara and Kohara 2014), myopia (Norton et al. 2006), stress-related disorders (Czeh et al. 2005; Fuchs 2005), and pharmacological tests (Zhao et al. 2014).
... However, brain regions activated in response to the aversive stimulus are still unclear in tree shrews. Previous studies have provided anatomically comprehensive maps of the tree shrew brain [13,15,30]. Therefore, the present study aimed to assess aversive valence maps encoding negative events in the forebrain of tree shrews by c-Fos immunohistochemistry. Also, we examined different patterns of c-Fos expression in the forebrain of tree shrews after acute restraint and footshock stress. ...
... All digital images of brain sections were adjusted for cropping, brightness/contrast, and image size using Adobe Photoshop CS6 (Adobe Systems, USA). The schematic drawings of the brain structures were adapted from the corresponding atlas panels in The Tree Shrew (Tupaia belangeri chinensis) Brain in Stereotaxic Coordinates [30]. For quantitative analysis of the density of c-Fos-ir nuclear profiles, more than fifteen sections at about 240-µm intervals from each animal were chosen for this study (one sixth of the forebrain sections). ...
... The morphology and location of the forebrain were delineated and identified according to our Nissl staining data ( Fig. 1) and in reference to the tree shrew brain atlas [30]. We applied immunohistochemistry to visualize neural responses to restraint and footshock stress. ...
The tree shrew is susceptible to stimuli. However, mapping of c-Fos expression in male tree shrew forebrain has not been explored. The present results provided the first detailed mapping of c-Fos expression in the forebrain of the tree shrew (Tupaia belangeri chinensis). Acute restraint stress rapidly increased the density of c-Fos-immunoreactive (-ir) neurons in the medial orbital cortex (MO), infralimbic cortex, intermediate part of the lateral septal nucleus (LSi), ventral part of the lateral septal nucleus (LSv), anterior part of the bed nucleus of the stria terminalis, posterior part of the bed nucleus of the stria terminalis (STP), paraventricular nucleus of the hypothalamus, supraoptic nucleus, lateral hypothalamic area, ventromedial hypothalamic nucleus (VMH), and medial amygdaloid nucleus (MeA). Furthermore, a significant increase in c-Fos expression was observed in the MO, LSi, LSv, STP, VMH, arcuate hypothalamic nucleus, anterior amygdaloid area, MeA, and cortical amygdaloid nucleus immediately after acute footshock stress. In addition, the distinct patterns of c-Fos expression in the forebrain were shown in context-, restraint-, or footshock-treated tree shrews. In general, the present study provides the first detailed maps of c-Fos expression in male tree shrew forebrain immediately after various stimuli.
... The total distance was analysed by ANY-maze. 30 and applied dental cement to fix the cannulas. ...
The progressively increased motivation for cocaine during abstinence is closely associated with the dysfunction of dopamine (DA) system. As DA receptors also dynamically regulate L‐type calcium channels (LTCCs), in this study we examined how DA receptors (D1R or D2R) and LTCCs (Cav1.2 or Cav1.3) exert their influences on cocaine‐seeking in a tree shrew (Tupaia belangeri chinensis) model. First, we demonstrated the ‘incubation’ effect by showing tree shrews exhibited a significantly higher seeking behaviour on withdrawal day (WD) 45 than on WD1. Then, we confirmed that longer abstinence period induced higher D1R expression in the nucleus accumbens (NAc). Next, we showed that LTCCs in the NAc participated in drug seeking. Moreover, Cav1.2 expression in the NAc was increased on WD45, and disruption of the Cav1.2 inhibited drug seeking. Finally, we found that D1R antagonist blocked the increase of Cav1.2 on drug‐seeking test. Collectively, these findings suggest that D1R‐mediated upregulation of Cav1.2 is involved in the incubation of cocaine craving. In this study, we reported the ‘incubation of cocaine craving’ phenomenon in tree shrews, a species that has a close gene affinity and shares similar characteristics of striatum between primates. Moreover, we found Cav1.2, rather than Cav1.3, in the nucleus accumbens played an important role in regulating drug‐seeking after long‐term withdrawal. At last, we found that Cav1.2 was upregulated by D1R during the seeking test, indicating that D1R‐mediated upregulation of Cav1.2 was involved in the incubation of cocaine.
... To date, several cytoarchitectonic atlases of large brains have been established with the aid of magnetic resonance imaging for stereotaxic coordinates, including for tree shrew (Tupaia belangeri chinensis) (Zhou and Ni, 2016), ferret (Mustela putorius furo) (Radtke-Schuller, 2018), common marmoset (Callithrix jacchus) (Yuasa et al., 2010;Paxinos et al., 2012;Liu et al., 2018), and rhesus monkey (Macaca mulatta) (Paxinos et al., 2008;Saleem and Logothetis, 2012;Reveley et al., 2017). However, the low-resolution data thus obtained, especially during continuous 3D scanning and analysis, do not reveal fine structures. ...
Mapping the cytoarchitecture of the whole brain can reveal the organizational logic of neural systems. However, this remains a significant challenge, especially for gyrencephalic brains with a large volume. Here we propose an integrated pipeline for generating a cytoarchitectonic atlas with single-cell resolution of the whole brain. To analyze a large-volume brain, we used a modified en-bloc Nissl staining protocol to achieve uniform staining of large-scale brain specimens from ferret (Mustela putorius furo). By combining whole-brain imaging and big data processing, we established strategies for parsing cytoarchitectural information at a voxel resolution of 0.33 μm × 0.33 μm × 1 μm and terabyte-scale data analysis. Using the cytoarchitectonic datasets for adult ferret brain, we identified giant pyramidal neurons in ferret brains and provide the first report of their morphological diversity, neurochemical phenotype, and distribution patterns in the whole brain in three dimensions. This pipeline will facilitate studies on the organization and development of the mammalian brains, from that of rodents to the gyrencephalic brains of ferret and even primates.
Impairments in spatial navigation in humans can be preclinical signs of Alzheimer's disease. Therefore, cognitive tests that monitor deficits in spatial memory play a crucial role in evaluating animal models with early stage Alzheimer's disease. While Chinese tree shrews (Tupaia belangeri) possess many features suitable for Alzheimer's disease modeling, behavioral tests for assessing spatial cognition in this species are lacking. Here, we established reward-based paradigms using the radial-arm maze and cheeseboard maze for tree shrews, and tested spatial memory in a group of 12 adult males in both tasks, along with a control water maze test, before and after bilateral lesions to the hippocampus, the brain region essential for spatial navigation. Tree shrews memorized target positions during training, and task performance improved gradually until reaching a plateau in all 3 mazes. However, spatial learning was compromised post-lesion in the 2 newly developed tasks, whereas memory retrieval was impaired in the water maze task. These results indicate that the cheeseboard task effectively detects impairments in spatial memory and holds potential for monitoring progressive cognitive decline in aged or genetically modified tree shrews that develop Alzheimer's disease-like symptoms. This study may facilitate the utilization of tree shrew models in Alzheimer's disease research.
The interpretation of early primate endocasts can be framed around four critical questions: (1) What are accurate estimates of endocranial capacity for known euprimate specimens? (2) What does the available data for stem primates tell us with respect to the earliest phases of primate brain evolution? (3) How should relative brain size be assessed? and (4) What is the appropriate comparative context for interpreting fossil primate endocasts? The widespread availability of CT data has allowed for better estimates of endocranial volume (#1), and for more data from stem primates (#2). From these data it is clear that the earliest primates had brains that were little differentiated in terms of form or size from their ancestors, although there might have been some modest increase in the relative size of the neocortex. Major changes in shape occurred at the euprimate node, with expansions in the temporal and occipital lobes (reflected in an expanded neocortex), and a lack of expansion in the olfactory bulbs. The brain of early fossil euprimates nonetheless still displayed primitive features such as narrow frontal lobes. Questions #3 and #4 remain contentious, although a much-expanded comparative sample of fossil endocasts allows for new perspectives on these issues.
Day-active tree shrews have a well-developed internal capsule (ic) that clearly separates the caudate nucleus (Cd) and putamen (Pu). The striatum consists of the Cd, ic, Pu, and accumbens nucleus (Acb). Here, we characterized the cytoarchitecture of the striatum and the whole-brain inputs to the Cd, Pu, and Acb in tree shrews by using immunohistochemistry and the retrograde tracer Fluoro-Gold (FG). Our data show the distribution patterns of parvalbumin (PV), nitric oxide synthase (NOS), calretinin (CR), and tyrosine hydroxylase (TH) immunoreactivity in the striatum of tree shrews, which were different from those observed in rats. The Cd and Pu mainly received inputs from the thalamus, motor cortex, somatosensory cortex, subthalamic nucleus, substantia nigra, and other cortical and subcortical regions, whereas the Acb primarily received inputs from the anterior olfactory nucleus, claustrum, infralimbic cortex, thalamus, raphe nucleus, parabrachial nucleus, ventral tegmental area, and so on. The Cd, Pu, and Acb received inputs from different neuronal populations in the ipsilateral (60, 67, and 63 brain regions, respectively) and contralateral (23, 20, and 36 brain regions, respectively) brain hemispheres. Overall, we demonstrate that there are species differences between tree shrews and rats in the density of PV, NOS, CR, and TH immunoreactivity in the striatum. Additionally, we mapped for the first time the distribution of whole-brain input neurons projecting to the striatum of tree shrews with FG injected into the Cd, Pu, and Acb. The similarities and differences in their brain-wide input patterns may provide new insights into the diverse functions of the striatal subregions.
Sex differences in behaviour partly arise from the sexual dimorphism of brain anatomy between males and females. However, the sexual dimorphism of the tree shrew brain is unclear. In the present study, we examined the detailed distribution of vasoactive intestinal polypeptide-immunoreactive (VIP-ir) neurons and fibres in the suprachiasmatic nucleus (SCN) and VIP-ir fibres in the bed nucleus of the stria terminalis (BST) of male and female tree shrews. The overall volume of the SCN in male tree shrews was comparable with that in females. However, males showed a significantly higher density of VIP-ir cells and fibres in the SCN than females. The shape of the VIP-stained area in coronal sections was arched, elongated or oval in the lateral division (STL) and the anterior part of the medial division (STMA) of the BST and oval or round in the posterior part of the medial division of the BST (STMP). The volume of the VIP-stained BST in male tree shrews was similar to that in females. The overall distribution of VIP-ir fibres was similar between the sexes throughout the BST except within the STMA, where darkly stained fibres were observed in males, whereas lightly stained fibres were observed in females. Furthermore, male tree shrews showed a significantly higher intensity of Nissl staining in the medial preoptic area (MPA) and the ventral part of the medial division of the BST than females. These findings are the first to reveal sexual dimorphism in the SCN, BST and MPA of the tree shrew brain, providing neuroanatomical evidence of sexual dimorphism in these regions related to their roles in sex differences in physiology and behaviour.
The gut and brain interact constantly in a complex fashion. Its intricacy and intrigue is progressively being revealed in the study of the “gut–brain axis”. Among many factors, abnormal light exposure is a potential powerful stressor, which is becoming ever more pervasive in our modern society. However, little is known about how stress, induced by staying up late by light, affects the gut–brain axis. We addressed this question by extending the normal circadian light for four hours at night in fifteen male tree shrews to simulate the pattern of staying up late in humans. The behavior, biochemical tests, microbiota dynamics, and brain structure of tree shrews were evaluated. The simple prolongation of light in the environment resulted in substantial changes of body weight loss, behavioral differences, total sleep time reduction, and an increased level of urine cortisol. These alterations were rescued by the treatment of either ketamine or washed microbiota transplantation (WMT). Importantly, the sustainability of WMT effect was better than that of ketamine. Magnetic Resonance Imaging analysis indicated that ketamine acted on the hippocampus and thalamus, and WMT mainly affected the piriform cortex and lateral geniculate nucleus. In conclusion, long-term light stimulation could change the behaviors, composition of gut microbiota and brain structure in tree shrews. Targeting microbiota thus certainly holds promise as a treatment for neuropsychiatric disorders, including but not limited to stress-related diseases.
The stereotaxic brain atlas is a fundamental reference tool commonly used in the field of neuroscience. Here we provide a brief history of brain atlas development and clarify three key conceptual elements of stereotaxic brain atlasing: brain image, atlas, and stereotaxis. We also refine four technical indices for evaluating the construction of atlases: the quality of staining and labeling, the granularity of delineation, spatial resolution, and the precision of spatial location and orientation. Additionally, we discuss state-of-the-art technologies and their trends in the fields of image acquisition, stereotaxic coordinate construction, image processing, anatomical structure recognition, and publishing: the procedures of brain atlas illustration. We believe that the use of single-cell resolution and micron-level location precision will become a future trend in the study of the stereotaxic brain atlas, which will greatly benefit the development of neuroscience.
Double staining protocols using the most popular immunoperoxidase techniques may raise difficulties. The two ordinary detection systems may cross-talk, when the primary antibodies are derived from phylogenetically closely related animals. A color shift of the 3,3′-diaminobenzidine (DAB) polymer may occur during the second development, resulting in poor distinction between the two kinds of deposits. A post-DAB technique, sulfide-silver-gold intensification, was fine tuned to eliminate these difficulties, which may be especially suitable for colocalization of cell nuclei and perikarya of the same cells. The revised method was probed in combination with a subsequent other immunoperoxidase step or fluorochrome-tagged reagents. The nuclear antigens (BrdU, c-Fos, and Prox-1) were first visualized with DAB polymer, which were then treated with SSGI, turning the deposit black. Thereafter, cytoplasmic antigens (doublecortin, neuronal nuclei, and calbindin) were detected with either another immunoperoxidase using DAB again or immunofluorescence labeling. In both approaches, the immunopositive nuclei and cytoplasmic sites could be easily distinguished even at low magnifications. Different shielding or eluting posttreatments were compared for consecutive acetylcholinesterase histochemistry terminated with DAB development and immunohistochemistry in the same sections. In conclusion, we recommend post-DAB treatments that abolish interactions between detection systems and allow clear distinction between the two signals under various conditions:
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