Fast prenatal development of the NPY neuron system in the neocortex of the European wild boar, Sus scrofa
Knowledge on cortical development is based mainly on small rodents besides primates and carnivores, all being altricial nestlings. Ungulates are precocial and born with nearly mature sensory and motor systems. Almost no information is available on ungulate brain development. Here, we analyzed European wild boar cortex development, focusing on the neuropeptide Y immunoreactive (NPY-ir) neuron system in dorsoparietal cortex from E35 to P30. Transient NPY-ir neuron types including archaic cells of the cortical plate and axonal loop cells of the subplate which appear by E60 concurrent with the establishment of the ungulate brain basic sulcal pattern. From E70, NPY-ir axons have an axon initial segment which elongates and shifts closer towards the axon’s point of origin until P30. From E85 onwards (birth at E114), NPY-ir neurons in cortical layers form basket cell-like local and Martinotti cell-like ascending axonal projections. The mature NPY-ir pattern is recognizable at E110. Together, morphologies are conserved across species, but timing is not: in pig, the adult pattern largely forms prenatally.
KeywordsTransient neuropeptide Y neurons NeuN Glutamate decarboxylase Gyration Body and organ weight
We acknowledge the Regionalverband Ruhr, Essen, Germany, for the interest in our work. We thank Dr. Oliver Keuling, TiHo Hannover, Germany, for advice with staging. We thank Andrea Räk, Sabine Schönfelder, Christian Riedel and Silke Vorwald for technical support. This research received no specific funding.
GM and PW conceived the experiments. CB and CB sampled the fetal material. LE, SD, JR, ME, MGG, GM and PW performed experiments or supplied tools for analysis. LE, GM and PW analyzed data and wrote the manuscript. All authors approved the manuscript.
Compliance with ethical standards
Conflict of interest
The corresponding author, on behalf of the coauthors, declares no conflict of interest.
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
- Andersen F, Watanabe H, Bjarkam C, Danielsen EH, Cumming P (2005) Pig brain stereotaxic standard space: mapping of cerebral blood flow normative values and effect of MPTP-lesioning. Brain Res Bull 66:17–29. https://doi.org/10.1016/j.brainresbull.2005.02.033 CrossRefPubMedGoogle Scholar
- Atapour N, Rosa MGP (2017) Age-related plasticity of the axon initial segment of cortical pyramidal cells in marmoset monkeys. Neurobiol Aging 57:95–103. https://doi.org/10.1016/j.neurobiolaging.2017.05.013 CrossRefPubMedGoogle Scholar
- Baker EW, Platt SR, Lau VW, Grace HE, Holmes SP, Wang L, Duberstein KJ, Howerth EW, Kinder HA, Stice SL, Hess DC, Mao H, West FD (2017) Induced pluripotent stem cell-derived neural stem cell therapy enhances recovery in an ischemic stroke pig model. Sci Rep 7:10075. https://doi.org/10.1038/s41598-017-10406-x CrossRefPubMedPubMedCentralGoogle Scholar
- Brauer K, Schober W (1970) Katalog der Säugetiergehirne: catalogue of mammalian brains. VEB Gustav Fischer Verlag, JenaGoogle Scholar
- Campbell AW (1905) Histological studies on the localisation of cerebral function. Cambridge University Press, CambridgeGoogle Scholar
- Corvino V, Marchese E, Giannetti S, Lattanzi W, Bonvissuto D, Biamonte F, Mongiovì AM, Michetti F, Geloso MC (2012) The neuroprotective and neurogenic effects of neuropeptide Y administration in an animal model of hippocampal neurodegeneration and temporal lobe epilepsy induced by trimethyltin. J Neurochem 122:415–426. https://doi.org/10.1111/j.1471-4159.2012.07770.x CrossRefPubMedGoogle Scholar
- Engelhardt M, Di Cristo G, Berardi N, Maffei L, Wahle P (2007) Differential effects of NT-4, NGF and BDNF on development of neurochemical architecture and cell size regulation in rat visual cortex during the critical period. Eur J Neurosci 25:529–540. https://doi.org/10.1111/j.1460-9568.2006.05301.x CrossRefPubMedGoogle Scholar
- Finney EM, Stone JR, Shatz CJ (1998) Major glutamatergic projection from subplate into visual cortex during development. J Comp Neurol 398:105–118. https://doi.org/10.1002/(SICI)1096-9861(19980817)398:1%3C105:AID-CNE7%3E3.0.CO;2-5 CrossRefPubMedGoogle Scholar
- Grate LL, Golden JA, Hoopes PJ, Hunter JV, Duhaime A-C (2003) Traumatic brain injury in piglets of different ages: techniques for lesion analysis using histology and magnetic resonance imaging. J Neurosci Methods 123:201–206. https://doi.org/10.1016/S0165-0270(02)00361-8 CrossRefPubMedGoogle Scholar
- Höfflin F, Jack A, Riedel C, Mack-Bucher J, Roos J, Corcelli C, Schultz C, Wahle P, Engelhardt M (2017) Heterogeneity of the axon initial segment in interneurons and pyramidal cells of rodent visual cortex. Front Cell Neurosci 11:332. https://doi.org/10.3389/fncel.2017.00332 CrossRefPubMedPubMedCentralGoogle Scholar
- Hökfelt T, Stanic D, Sanford SD, Gatlin JC, Nilsson I, Paratcha G, Ledda F, Fetissov S, Lindfors C, Herzog H, Johansen JE, Ubink R, Pfenninger KH (2008) NPY and its involvement in axon guidance, neurogenesis, and feeding. Nutrition 24:860–868. https://doi.org/10.1016/j.nut.2008.06.010 CrossRefPubMedGoogle Scholar
- Jamann N, Jordan M, Engelhardt M (2018) Activity-dependent axonal plasticity in sensory systems. Neuroscience 368:268–282. https://doi.org/10.1016/j.neuroscience.2017.07.035 CrossRefPubMedGoogle Scholar
- Kanold PO, Luhmann HJ (2010) The subplate and early cortical circuits. Annu Rev Neurosci 33:23–48. https://doi.org/10.1146/annurev-neuro-060909-153244 CrossRefPubMedGoogle Scholar
- Klassen H, Kiilgaard JF, Warfvinge K, Samuel MS, Prather RS, Wong F, Petters RM, La Cour M, Young MJ (2012) Photoreceptor differentiation following transplantation of allogeneic retinal progenitor cells to the dystrophic rhodopsin Pro347Leu transgenic pig. Stem Cells Int 2012:939801. https://doi.org/10.1155/2012/939801 CrossRefPubMedPubMedCentralGoogle Scholar
- Lin Y-S, Wang H-Y, Huang D-F, Hsieh P-F, Lin M-Y, Chou C-H, Wu I-J, Huang G-J, Gau SS-F, Huang H-S (2016) Neuronal splicing regulator RBFOX3 (NeuN) regulates adult hippocampal neurogenesis and synaptogenesis. PLoS One 11:e0164164. https://doi.org/10.1371/journal.pone.0164164 CrossRefPubMedPubMedCentralGoogle Scholar
- Mc-Phearson-McCassidy RL (2003) Fetal growth and development of the pig. M.Sc. Thesis, Texas Tech University. http://hdl.handle.net/2346/8522
- Neef J (2009) Untersuchungen zur Reproduktionsdynamik beim mitteleuropäischen Wildschwein, Edition scientifique, 1 Aufl. VVB Laufersweiler, GiessenGoogle Scholar
- Nickel R, Schummer A, Seiferle E (1991) Lehrbuch der Anatomie der Haustiere. B and IV: Nervensystem, Sinnesorgane, Endokrine Drüsen. Parey, BerlinGoogle Scholar
- Qu G-J, Ma J, Yu Y-C, Fu Y (2016) Postnatal development of GABAergic interneurons in the neocortical subplate of mice. Neuroscience 322:78–93. https://doi.org/10.1016/j.neuroscience.2016.02.023 CrossRefPubMedGoogle Scholar
- Sakoh M, Ostergaard L, Gjedde A, Røhl L, Vestergaard-Poulsen P, Smith DF, Le Bihan D, Sakaki S, Gyldensted C (2001) Prediction of tissue survival after middle cerebral artery occlusion based on changes in the apparent diffusion of water. J Neurosurg 95:450–458. https://doi.org/10.3171/jns.2001.95.3.0450 CrossRefPubMedGoogle Scholar
- Schmidt V (2015) Comparative anatomy of the pig brain: an integrative magnetic resonance imaging (MRI) study of the porcine brain with special emphasis on the external morphology of the cerebral cortex, 1. Aufl. Edition scientifique. Laufersweiler, GiessenGoogle Scholar
- Smith DH, Chen X-H, Nonaka M, Trojanowski JQ, Lee V-Y, Saatman KE, Leoni MJ, Xu B-N, Wolf JA, Meaney DF (1999) Accumulation of amyloid β and tau and the formation of neurofilament inclusions following diffuse brain injury in the pig. J Neuropathol Exp Neurol 58:982–992. https://doi.org/10.1097/00005072-199909000-00008 CrossRefPubMedGoogle Scholar
- Sweasey D, Patterson DSP, Glancy EM (1976) Biphasic myelination and the fatty acid composition of cerebrosides and cholesterol esters in the developing central nervous system of the domestic pig. J Neurochem 27:375–380. https://doi.org/10.1111/j.1471-4159.1976.tb12256.x CrossRefPubMedGoogle Scholar
- Uylings H, Delalle I (1997) Morphology of neuropeptide Y-immunoreactive neurons and fibers in human prefrontal cortex during prenatal and postnatal development. J Comp Neurol. https://doi.org/10.1002/(SICI)1096-9861(19970324)379:43.0.CO;2-4 CrossRefPubMedGoogle Scholar
- Wahle P, Meyer G, Wu J-Y, Albus K (1987) Morphology and axon terminal pattern of glutamate decarboxylase-immunoreactive cell types in the white matter of the cat occipital cortex during early postnatal development. Dev Brain Res 36:53–61. https://doi.org/10.1016/0165-3806(87)90064-2 CrossRefGoogle Scholar
- Yue X, Mehmet H, Penrice J, Cooper C, Cady E, Wyatt JS, Reynolds EOR, Edwards AD, Squier MV (1997) Apoptosis and necrosis in the newborn piglet brain following transient cerebral hypoxia–ischaemia. Neuropathol Appl Neurobiol 23:16–25. https://doi.org/10.1111/j.1365-2990.1997.tb01181.x CrossRefPubMedGoogle Scholar