Dataset Information

Single-axon level morphological analysis of corticofugal projection neurons in mouse barrel field.

ABSTRACT: Corticofugal projection neurons are key components in connecting the neocortex and the subcortical regions. In the barrel field, these neurons have various projection targets and play crucial roles in the rodent whisker sensorimotor system. However, the projection features of corticofugal projection neurons at the single-axon level are far from comprehensive elucidation. Based on a brain-wide positioning system with high-resolution imaging for Thy1-GFP M-line mice brains, we reconstructed and analyzed more than one hundred corticofugal projection neurons in both layer V and VI of barrel cortex. The dual-color imaging made it possible to locate the neurons' somata, trace their corresponding dendrites and axons and then distinguish the neurons as L5 type I/II or L6 type. The corticofugal projection pattern showed significant diversity across individual neurons. Usually, the L5 type I neurons have greater multi-region projection potential. The thalamus and the midbrain are the most frequent projection targets among the investigated multidirectional projection neurons, and the hypothalamus is particularly unique in that it only appears in multidirectional projection situations. Statistically, the average branch length of apical dendrites in multi-region projection groups is larger than that of single-region projection groups. This study demonstrated a single-axon-level analysis for barrel corticofugal projection neurons, which could provide a micro-anatomical basis for interpreting whisker sensorimotor circuit function.

SUBMITTER: Guo C

PROVIDER: S-EPMC5460143 | biostudies-literature | 2017 Jun

REPOSITORIES: biostudies-literature

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Single-axon level morphological analysis of corticofugal projection neurons in mouse barrel field.

Guo Congdi C Peng Jie J Zhang Yalun Y Li Anan A Li Yuxin Y Yuan Jing J Xu Xiaofeng X Ren Miao M Gong Hui H Chen Shangbin S

Scientific reports 20170606 1

Corticofugal projection neurons are key components in connecting the neocortex and the subcortical regions. In the barrel field, these neurons have various projection targets and play crucial roles in the rodent whisker sensorimotor system. However, the projection features of corticofugal projection neurons at the single-axon level are far from comprehensive elucidation. Based on a brain-wide positioning system with high-resolution imaging for Thy1-GFP M-line mice brains, we reconstructed and an ...[more]

PMID: 28588276

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Project description:Pathways arising from the ventral tegmental area (VTA) release dopamine and other neurotransmitters during the expectation and achievement of reward, and are regarded as central links of the brain networks that create drive, pleasure, and addiction. While the global pattern of VTA projections is well-known, the actual axonal wiring of individual VTA neurons had never been investigated. Here, we labeled and analyzed the axons of 30 VTA single neurons by means of single-cell transfection with the Sindbis-pal-eGFP vector in mice. These observations were complemented with those obtained by labeling the axons of small populations of VTA cells with iontophoretic microdeposits of biotinylated dextran amine. In the single-cell labeling experiments, each entire axonal tree was reconstructed from serial sections, the length of terminal axonal arbors was estimated by stereology, and the dopaminergic phenotype was tested by double-labeling for tyrosine hydroxylase immunofluorescence. We observed two main, markedly different VTA cell morphologies: neurons with a single main axon targeting only forebrain structures (FPN cells), and neurons with multibranched axons targeting both the forebrain and the brainstem (F + BSPN cells). Dopaminergic phenotype was observed in FPN cells. Moreover, four "subtypes" could be distinguished among the FPN cells based on their projection targets: (1) "Mesocorticolimbic" FPN projecting to both neocortex and basal forebrain; (2) "Mesocortical" FPN innervating the neocortex almost exclusively; (3) "Mesolimbic" FPN projecting to the basal forebrain, accumbens and caudateputamen; and (4) "Mesostriatal" FPN targeting only the caudateputamen. While the F + BSPN cells were scattered within VTA, the mesolimbic neurons were abundant in the paranigral nucleus. The observed diversity in wiring architectures is consistent with the notion that different VTA cell subpopulations modulate the activity of specific sets of prosencephalic and brainstem structures.

Project description:Projection neurons are the commonest neuronal type in the mammalian forebrain and their individual characterization is a crucial step to understand how neural circuitry operates. These cells have an axon whose arborizations extend over long distances, branching in complex patterns and/or in multiple brain regions. Axon length is a principal estimate of the functional impact of the neuron, as it directly correlates with the number of synapses formed by the axon in its target regions; however, its measurement by direct 3D axonal tracing is a slow and labor-intensive method. On the contrary, axon length estimations have been recently proposed as an effective and accessible alternative, allowing a fast approach to the functional significance of the single neuron. Here, we analyze the accuracy and efficiency of the most used length estimation tools-design-based stereology by virtual planes or spheres, and mathematical correction of the 2D projected-axon length-in contrast with direct measurement, to quantify individual axon length. To this end, we computationally simulated each tool, applied them over a dataset of 951 3D-reconstructed axons (from NeuroMorpho.org), and compared the generated length values with their 3D reconstruction counterparts. The evaluated reliability of each axon length estimation method was then balanced with the required human effort, experience and know-how, and economic affordability. Subsequently, computational results were contrasted with measurements performed on actual brain tissue sections. We show that the plane-based stereological method balances acceptable errors (~5%) with robustness to biases, whereas the projection-based method, despite its accuracy, is prone to inherent biases when implemented in the laboratory. This work, therefore, aims to provide a constructive benchmark to help guide the selection of the most efficient method for measuring specific axonal morphologies according to the particular circumstances of the conducted research.

Dataset Information

Single-axon level morphological analysis of corticofugal projection neurons in mouse barrel field.

Publications

Single-axon level morphological analysis of corticofugal projection neurons in mouse barrel field.

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