Single-neuron projectomes of mouse paraventricular hypothalamic nucleus oxytocin neurons reveal mutually exclusive projection patterns

Li, Humingzhu; Jiang, Tao; An, Sile; Xu, Mingrui; Gou, Lingfeng; Ren, Biyu; Shi, Xiaoxue; Wang, Xiaofei; Yan, Jun; Yuan, Jing; Xu, Xiaohong; Wu, Qing-Feng; Luo, Qingming; Gong, Hui; Bian, Wen-Jie; Li, Anan; Yu, Xiang

doi:10.1016/j.neuron.2023.12.022

Cited by 10 publications

(1 citation statement)

References 82 publications

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“…Arrows indicate cells that are double-positive for Myc and OT. This area corresponds to the posterior part of the PVH where parvocellular PVH OT neurons projecting the SC present 65 . b , Coronal section of the spinal cord segment showing the expression of Chat (magenta) and c-Fos (green) in IML region following CNO administration in Otr-Cre mice injected with AAV5- OTp - Gq-Myc or AV9- OTp - mCherry into the PVH.…”

Section: Extended Data Figures and Legendsmentioning

confidence: 99%

Parallel Labeled-Line Organization of Sympathetic Outflow for Selective Organ Regulation in Mice

Harima,

Tsurutani,

Uchida

et al. 2024

Preprint

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The sympathetic nervous system is vital in maintaining homeostasis and responding to environmental changes1–3. This regulation is coordinated by the spinal sympathetic preganglionic neurons (SPNs), which influence various organs both through neuronal pathways via postganglionic neurons and through endocrine processes by innervating the adrenal gland. Despite decades of research supporting the concept of selective control within this system1,4–9, the neural circuit organization responsible for the specificity of sympathetic outflow remains poorly understood. Notably, classical anatomical studies in rats have not revealed a definitive molecular code governing SPNs, nor have they confirmed the existence of SPNs strictly corresponding to specific output targets1,6,10,11. To reconcile this discrepancy, we aim to integrate recent transcriptome data of SPNs12,13in mice with viral-genetic toolkits14to map axonal projections and manipulate the functions of SPNs governing the gastrointestinal tract and adrenal gland. Here, we have identified two subtypes of SPNs in the lower thoracic spinal cord, defined at the molecular level, exhibiting non-overlapping patterns of innervation. Chemogenetic manipulations on these distinct SPN subtypes revealed selective impacts on the digestive functions in the gastrointestinal tracts or glucose metabolism mediated by the adrenal gland, respectively. This molecularly delineated parallel labeled-line organization in sympathetic outflows presents a potential avenue for selectively manipulating organ functions.

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Section: Extended Data Figures and Legendsmentioning

confidence: 99%

Parallel Labeled-Line Organization of Sympathetic Outflow for Selective Organ Regulation in Mice

Harima,

Tsurutani,

Uchida

et al. 2024

Preprint

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The central oxytocinergic system of the prairie vole

Ramos,

Jiron,

Danoff

et al. 2024

Brain Struct Funct

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Oxytocin (OXT) is a peptide hormone and a neuropeptide that regulates various peripheral physiological processes and modulates behavioral responses in the central nervous system. While the humoral release occurs from the axons arriving at the median eminence, the neuropeptide is also released from oxytocinergic cell axons in various brain structures that contain its receptor, and from their dendrites in hypothalamic nuclei and potentially into the cerebrospinal fluid (CSF). Understanding oxytocin’s complex functions requires the knowledge on patterns of oxytocinergic projections in relationship to its receptor (OXTR). This study provides the first comprehensive examination of the oxytocinergic system in the prairie vole (Microtus ochrogaster), an animal exhibiting social behaviors that mirror human social behaviors linked to oxytocinergic functioning. Using light and electron microscopy, we characterized the neuroanatomy of the oxytocinergic system in this species. OXT+ cell bodies were found primarily in the hypothalamus, and axons were densest in subcortical regions. Examination of the OXT+ fibers and their relationship to oxytocin receptor transcripts (Oxtr) revealed that except for some subcortical structures, the presence of axons was not correlated with the amount of Oxtr across the brain. Of particular interest, the cerebral cortex that had high expression of Oxtr transcripts contained little to no fibers. Electron microscopy is used to quantify dense cored vesicles (DCV) in OXT+ axons and to identify potential axonal release sites. The ependymal cells that line the ventricles were frequently permissive of DCV-containing OXT+ dendrites reaching the third ventricle. Our results highlight a mechanism in which oxytocin is released directly into the ventricles and circulates throughout the ventricular system, may serve as the primary source for oxytocin that binds to OXTR in the cerebral cortex.

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Spatiotemporal Mapping of the Oxytocin Receptor at Single-Cell Resolution in the Postnatally Developing Mouse Brain

Li,

Wang

et al. 2024

Neurosci. Bull.

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The oxytocin receptor (OXTR) has garnered increasing attention for its role in regulating both mature behaviors and brain development. It has been established that OXTR mediates a range of effects that are region-specific or period-specific. However, the current studies of OXTR expression patterns in mice only provide limited help due to limitations in resolution. Therefore, our objective was to generate a comprehensive, high-resolution spatiotemporal expression map of Oxtr mRNA across the entire developing mouse brain. We applied RNAscope in situ hybridization to investigate the spatiotemporal expression pattern of Oxtr in the brains of male mice at six distinct postnatal developmental stages (P7, P14, P21, P28, P42, P56). We provide detailed descriptions of Oxtr expression patterns in key brain regions, including the cortex, basal forebrain, hippocampus, and amygdaloid complex, with a focus on the precise localization of Oxtr+ cells and the variance of expression between different neurons. Furthermore, we identified some neuronal populations with high Oxtr expression levels that have been little studied, including glutamatergic neurons in the ventral dentate gyrus, Vgat+Oxtr+ cells in the basal forebrain, and GABAergic neurons in layers 4/5 of the cortex. Our study provides a novel perspective for understanding the distribution of Oxtr and encourages further investigations into its functions.

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Single-neuron projectomes of mouse paraventricular hypothalamic nucleus oxytocin neurons reveal mutually exclusive projection patterns

Cited by 10 publications

References 82 publications

Parallel Labeled-Line Organization of Sympathetic Outflow for Selective Organ Regulation in Mice

Parallel Labeled-Line Organization of Sympathetic Outflow for Selective Organ Regulation in Mice

The central oxytocinergic system of the prairie vole

Spatiotemporal Mapping of the Oxytocin Receptor at Single-Cell Resolution in the Postnatally Developing Mouse Brain

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