Fast prenatal development of the NPY neuron system in the neocortex of the European wild boar, Sus scrofa

Ernst, Laura; Darschnik, Simon; Roos, Johannes L.; González‐Gómez, Miriam; Beemelmans, Christa; Beemelmans, Christoph; Engelhardt, Maren; Meyer, Gundela; Wahle, Petra

doi:10.1007/s00429-018-1725-y

Cited by 21 publications

(33 citation statements)

References 75 publications

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“…AIS length and distance from the soma were obtained using a self-written program in Python (AISuite et al, unpublished; Hoefflin et al, 2017; Ernst et al, 2018). Briefly, in this application, the AIS is traced manually, beginning with the axon hillock and ending with the axon past visible AIS staining to exclude personal bias.…”

Section: Methodsmentioning

confidence: 99%

Dynamic Regulation of Synaptopodin and the Axon Initial Segment in Retinal Ganglion Cells During Postnatal Development

Schlüter

Roßberger

Dannehl

et al. 2019

Front. Cell. Neurosci.

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A key component allowing a neuron to function properly within its dynamic environment is the axon initial segment (AIS), the site of action potential generation. In visual cortex, AIS of pyramidal neurons undergo periods of activity-dependent structural plasticity during development. However, it remains unknown how AIS morphology is organized during development for downstream cells in the visual pathway (retinal ganglion cells; RGCs) and whether AIS retain the ability to dynamically adjust to changes in network state. Here, we investigated the maturation of AIS in RGCs during mouse retinal development, and tested putative activity-dependent mechanisms by applying visual deprivation with a focus on the AIS-specific cisternal organelle (CO), a presumed Ca 2+ -store. Whole-mount retinae from wildtype and Thy1-GFP transgenic mice were processed for multi-channel immunofluorescence using antibodies against AIS scaffolding proteins ankyrin-G, βIV-spectrin and the CO marker synaptopodin (synpo). Confocal microscopy in combination with morphometrical analysis of AIS length and position as well as synpo cluster size was performed. Data indicated that a subset of RGC AIS contains synpo clusters and that these show significant dynamic regulation in size during development as well as after visual deprivation. Using super resolution microscopy, we addressed the subcellular localization of synpo in RGC axons. Similar to cortical neurons, RGCs show a periodic distribution of AIS scaffolding proteins. A previously reported scaffold-deficient nanodomain correlating with synpo localization is not evident in all RGC AIS. In summary, our work demonstrates a dynamic regulation of both the AIS and synpo in RGCs during retinal development and after visual deprivation, providing first evidence that the AIS and CO in RGCs can undergo structural plasticity in response to changes in network activity.

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Section: Methodsmentioning

confidence: 99%

Dynamic Regulation of Synaptopodin and the Axon Initial Segment in Retinal Ganglion Cells During Postnatal Development

Schlüter

Roßberger

Dannehl

et al. 2019

Front. Cell. Neurosci.

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“…Fluorescence images were acquired using a Nikon C2 confocal microscope with 40× and 60× objectives (numerical aperture 1.4). AIS length was determined using the Python-based, self-written software AISuite as previously described [39][40][41]. The AISuite software is available via github.com/jhnnsrs/aisuite2.…”

Section: Immunofluorescence and Image Analysismentioning

confidence: 99%

Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons

Benedetti

Dannehl

Janssen

et al. 2020

IJMS

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Rodent neocortical neurons undergo prominent postnatal development and maturation. The process is associated with structural and functional maturation of the axon initial segment (AIS), the site of action potential initiation. In this regard, cell size and optimal AIS length are interconnected. In sensory cortices, developmental onset of sensory input and consequent changes in network activity cause phasic AIS plasticity that can also control functional output. In non-sensory cortices, network input driving phasic events should be less prominent. We, therefore, explored the relationship between postnatal functional maturation and AIS maturation in principal neurons of the primary motor cortex layer V (M1LV), a non-sensory area of the rat brain. We hypothesized that a rather continuous process of AIS maturation and elongation would reflect cell growth, accompanied by progressive refinement of functional output properties. We found that, in the first two postnatal weeks, cell growth prompted substantial decline of neuronal input resistance, such that older neurons needed larger input current to reach rheobase and fire action potentials. In the same period, we observed the most prominent AIS elongation and significant maturation of functional output properties. Alternating phases of AIS plasticity did not occur, and changes in functional output properties were largely justified by AIS elongation. From the third postnatal week up to five months of age, cell growth, AIS elongation, and functional output maturation were marginal. Thus, AIS maturation in M1LV is a continuous process that attunes the functional output of pyramidal neurons and associates with early postnatal development to counterbalance increasing electrical leakage due to cell growth.

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“…Inoculation at late gestation targets the initiation of the brain growth spurt, which begins in the last third of gestation and continues into the first several postnatal months (27,28). The gestational window investigated here (E76 to E97) is primarily characterized by ongoing innervation and synaptogenesis and the initiation of myelination (29)(30)(31)(32) and is ∼2 to 5 wk past the peak of neurogenesis (at E60), when the percent of immature neurons is rapidly declining (33,34). This timing corresponds to late prenatal neurodevelopmental stages of the human fetus (roughly 28 to 38 wk of human gestation) (35) and to the first 1 to 2 postnatal weeks in rodents (27,34,36,37).…”

Section: Significancementioning

confidence: 99%

Maternal viral infection causes global alterations in porcine fetal microglia

Antonson

Lawson

Caputo

et al. 2019

Proc. Natl. Acad. Sci. U.S.A.

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Maternal infections during pregnancy are associated with increased risk of neurodevelopmental disorders, although the precise mechanisms remain to be elucidated. Previously, we established a maternal immune activation (MIA) model using swine, which results in altered social behaviors of piglet offspring. These behavioral abnormalities occurred in the absence of microglia priming. Thus, we examined fetal microglial activity during prenatal development in response to maternal infection with live porcine reproductive and respiratory syndrome virus. Fetuses were obtained by cesarean sections performed 7 and 21 d postinoculation (dpi). MIA fetuses had reduced brain weights at 21 dpi compared to controls. Furthermore, MIA microglia increased expression of major histocompatibility complex class II that was coupled with reduced phagocytic and chemotactic activity compared to controls. High-throughput gene-expression analysis of microglial-enriched genes involved in neurodevelopment, the microglia sensome, and inflammation revealed differential regulation in primary microglia and in whole amygdala tissue. Microglia density was increased in the fetal amygdala at 7 dpi. Our data also reveal widespread sexual dimorphisms in microglial gene expression and demonstrate that the consequences of MIA are sex dependent. Overall, these results indicate that fetal microglia are significantly altered by maternal viral infection, presenting a potential mechanism through which MIA impacts prenatal brain development and function. maternal immune activation | microglia | neurodevelopment | prenatal inflammation | pig Author contributions: A.M.A., M.A.L., and R.W.J. designed research; A.M.A., M.A.L., M.P.C., S.M.M., and B.J.L. performed research; A.M.A., M.P.C., and S.M.M. analyzed data; A.M.A., M.A.L., and R.W.J. interpreted data; and A.M.A. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission.Published under the PNAS license. NEUROSCIENCEDownloaded by guest on July 10, 2020 3 symbols = P < 0.001, 2 symbols = P < 0.01, and 1 symbol = P < 0.05.Antonson et al.

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Fast prenatal development of the NPY neuron system in the neocortex of the European wild boar, Sus scrofa

Cited by 21 publications

References 75 publications

Dynamic Regulation of Synaptopodin and the Axon Initial Segment in Retinal Ganglion Cells During Postnatal Development

Dynamic Regulation of Synaptopodin and the Axon Initial Segment in Retinal Ganglion Cells During Postnatal Development

Structural and Functional Maturation of Rat Primary Motor Cortex Layer V Neurons

Maternal viral infection causes global alterations in porcine fetal microglia

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