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Molecular Brain Volume 15 ,Issue 1 ,2022-10-24
Preferential subcortical collateral projections of pedunculopontine nucleus-targeting cortical pyramidal neurons revealed by brain-wide single fiber tracing
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Qiao-Qiong Liu 1 Yu-Xiao Cheng 1 Qi Jing 1 Ke-Ming Zhang 1 Lu-Feng Ding 2 Xiao-Wei Fan 2 Chun-Hui Jia 1 Fang Xu 2 Guo-Qiang Bi 1 , 2 Pak-Ming Lau 1 , 2
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DOI:10.1186/s13041-022-00975-y
Received 2022-8-23, accepted for publication 2022-10-24, Published 2022-10-24
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摘要

The pedunculopontine nucleus (PPN) is a heterogeneous midbrain structure involved in various brain functions, such as motor control, learning, reward, and sleep. Previous studies using conventional tracers have shown that the PPN receives extensive afferent inputs from various cortical areas. To examine how these cortical axons make collateral projections to other subcortical areas, we used a dual-viral injection strategy to sparsely label PPN-targeting cortical pyramidal neurons in CaMKIIα-Cre transgenic mice. Using a high-speed volumetric imaging with on-the-fly-scan and Readout (VISoR) technique, we visualized brain-wide axonal projections of individual PPN-targeting neurons from several cortical areas, including the prelimbic region (PL), anterior cingulate area (ACA) and secondary motor cortex (MOs). We found that each PPN-projecting neuron had a unique profile of collateralization, with some subcortical areas being preferential targets. In particular, PPN-projecting neurons from all three traced cortical areas exhibited common preferential collateralization to several nuclei, with most neurons targeting the striatum (STR), lateral hypothalamic area (LHA) and periaqueductal gray (PAG), and a substantial portion of neurons also targeting the zona incerta (ZI), median raphe nucleus (MRN) and substantia nigra pars reticulata (SNr). Meanwhile, very specific collateralization patterns were found for other nuclei, including the intermediate reticular nucleus (IRN), parvicellular reticular nucleus (PARN) and gigantocellular reticular nucleus (GRN), which receive collateral inputs almost exclusively from the MOs. These observations provide potential anatomical mechanisms for cortical neurons to coordinate the PPN with other subcortical areas in performing different physiological functions.

关键词

VISoR whole-brain imaging;Motor cortex;Prelimbic region;Anterior cingulate area;Collateral projection;CaMKIIα-positive neuron;Pedunculopontine nucleus

授权许可

© The Author(s) 2022
Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

图表

Brain-wide inputs to the PPN and collateralization of PPN-targeting cortical pyramidal neurons. a Horizontal view from whole-brain VISoR imaging of excitatory neurons labeled by retrograde tracing virus (rAAV2-retro-EF1α-DIO-EGFP) injected into the PPN of a CaMKIIα-Cre transgenic mouse. Solid lines indicate cortical and subcortical areas to be examined in b and c-d, respectively. A: anterior; P: posterior; L: left; R: right; D: dorsal; V: ventral. b Maximum‑intensity projection of part of a 100 μm-thick coronal section encompassing the MOs, ACA, and PL (b1). Enlarged views of the boxed areas in b1 show EGFP-expressing PPN-targeting neurons in the MOs (b2), ACA (b3) and PL (b4). c, d Maximum-intensity projection of part of a coronal section encompassing the PAG (c1) and the PARN (d1). Enlarged views of the boxed areas in (c2) and (d2), showing labeled neurons in the PAG and PARN, respectively. e Diagrams of the cell type specific and target-specific sparse labeling of PPN-projecting cortical pyramidal neurons. f–h Imaging and 3D reconstruction of individual PPN-projecting neurons from the ACA (f), PL (g), and MOs (h), showing brain-wide axonal projections (f1, g1, h1) and dendritic morphologies (f2, f3, g2, g3, h2, h3) of sparsely labeled cortical neurons. Enlarged views of subcortical areas within the PAG (f4, f5), VTA (g4, g5), STR (h4, h5), and PPN (f6, f7, g6, g7, h6, h7) show termini of axonal collaterals from the traced cortical neurons. i Collateralization profile of individual pyramidal neurons in the ACA (n = 4), PL (n = 4) and MOs (n = 3). The heatmap shows the number of axon terminals made by each neuron. j Qualitative summary of subcortical collateralization from the three cortical areas. The collateralization ratio (CR, defined as the number of PPN-projecting neurons from a given cortical area making at least 2 terminals in a specified subcortical target area divided by the total number of neurons traced for this cortical area) is separated into 3 categories: “−” for CR = 0; “+” for CR ≤ 33.3%; “++” for 33.3% < CR < 66.7%; “+++” for CR ≥ 66.7%

通讯作者

1. Guo-Qiang Bi.Division of Life Sciences and Medicine, University of Science and Technology of China, 230026, Hefei, Anhui, China;Interdisciplinary Center for Brain Information, The Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, 518055, Shenzhen, Guangdong, China.gqbi@ustc.edu.cn
2. Pak-Ming Lau.Division of Life Sciences and Medicine, University of Science and Technology of China, 230026, Hefei, Anhui, China;Interdisciplinary Center for Brain Information, The Brain Cognition and Brain Disease Institute, Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences, 518055, Shenzhen, Guangdong, China.plau@ustc.edu.cn

推荐引用方式

Qiao-Qiong Liu,Yu-Xiao Cheng,Qi Jing,Ke-Ming Zhang,Lu-Feng Ding,Xiao-Wei Fan,Chun-Hui Jia,Fang Xu,Guo-Qiang Bi,Pak-Ming Lau. Preferential subcortical collateral projections of pedunculopontine nucleus-targeting cortical pyramidal neurons revealed by brain-wide single fiber tracing. Molecular Brain ,Vol.15, Issue 1(2022)

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参考文献
[1] ND Volkow, M Michaelides, R BalerThe neuroscience of drug reward and addictionPhysiol Rev2019992115214010.1152/physrev.00014.20183150724468909851:CAS:528:DC
[2] 2BB3cXitFWjsLc
[3] 3D
[4] RUAS Toor, Q-J Sun, NN Kumar, S Le et al.Neurons in the intermediate reticular nucleus coordinate postinspiratory activity, swallowing, and respiratory-sympathetic coupling in the ratJ Neurosci2019399757976610.1523/JNEUROSCI.0502-19.20193166635468910601:CAS:528:DC
[5] 2BB3cXjt1aqt7k
[6] 3D
[7] P Vázquez-León, A Miranda-Páez, J Chávez-Reyes, G Allende et al.The periaqueductal gray and its extended participation in drug addiction phenomenaNeurosci Bull2021371493150910.1007/s12264-021-00756-y343026188490541
[8] PG Anastasiades, AG CarterCircuit organization of the rodent medial prefrontal cortexTrends Neurosci20214455056310.1016/j.tins.2021.03.0063397210082221441:CAS:528:DC
[9] 2BB3MXpt12rtrc
[10] 3D
[11] J Cox, IB WittenStriatal circuits for reward learning and decision-makingNat Rev Neurosci20192048249410.1038/s41583-019-0189-23117183972312281:CAS:528:DC
[12] 2BC1MXhsVWjsb3L
[13] EE BenarrochPedunculopontine nucleus: functional organization and clinical implicationsNeurology2013801148115510.1212/WNL.0b013e3182886a7623509047
[14] H Yu, X Xiang, Z Chen, X Wang et al.Periaqueductal gray neurons encode the sequential motor program in hunting behavior of miceNat Commun202112652310.1038/s41467-021-26852-1347642798586038
[15] AK Engmann, F Bizzozzero, MP Schneider, D Pfyffer et al.The gigantocellular reticular nucleus plays a significant role in locomotor recovery after incomplete spinal cord injuryJ Neurosci2020408292830510.1523/JNEUROSCI.0474-20.20203297828975775991:CAS:528:DC
[16] 2BB3cXisF2lurvL
[17] D Mogoseanu, AD Smith, JP BolamMonosynaptic innervation of facial motoneurones by neurones of the parvicellular reticular formationExp Brain Res199410142743810.1007/BF0022733675316501:STN:280:DyaK2M7lsVChtg
[18] 3D
[19] 3D
[20] S Grillner, J Hellgren, A Ménard, K Saitoh et al.Mechanisms for selection of basic motor programs–roles for the striatum and pallidumTrends Neurosci20052836437010.1016/j.tins.2005.05.004159354871:CAS:528:DC
[21] 2BD2MXlsVequ78
[22] 3D
[23] L Gao, S Liu, L Gou, Y Hu et al.Single-neuron projectome of mouse prefrontal cortexNat Neurosci20222551552910.1038/s41593-022-01041-5353619731:CAS:528:DC
[24] 2BB38Xosl2hur0
[25] 3D
[26] M Özkan, B Köse, O Algın, S Oğuz et al.Non-motor connections of the pedunculopontine nucleus of the rat and human brainNeurosci Lett202276710.1016/j.neulet.2021.13630834715273
[27] KH Monakow, K Akert, H KünzleProjections of precentral and premotor cortex to the red nucleus and other midbrain areas in Macaca fascicularisExp Brain Res1979349110510.1007/BF00238343832421:STN:280:DyaE1M
[28] 2Fos1Sjsg
[29] 3D
[30] 3D
[31] R Muñoz-Castañeda, B Zingg, KS Matho, X Chen et al.Cellular anatomy of the mouse primary motor cortexNature202159815916610.1038/s41586-021-03970-w346160718494646
[32] PA Pahapill, AM LozanoThe pedunculopontine nucleus and Parkinson’s diseaseBrain J Neurol20001231767178310.1093/brain/123.9.1767