Brain Structure and Function

, Volume 223, Issue 8, pp 3855–3873 | Cite as

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

  • Laura Ernst
  • Simon Darschnik
  • Johannes Roos
  • Miriam González-Gómez
  • Christa Beemelmans
  • Christoph Beemelmans
  • Maren Engelhardt
  • Gundela Meyer
  • Petra WahleEmail author
Original Article


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.


Transient 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.

Author contributions

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.

Ethical approval

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.

Supplementary material

429_2018_1725_MOESM1_ESM.docx (15 kb)
Online resource 1. Reagents used for immunohistochemistry. (DOCX 15 KB)
429_2018_1725_MOESM2_ESM.jpg (2 mb)
Online resource 2. Representative fetuses and P30 boar piglet. Animals are shown at the same magnification. Note emergence of external features like the chin hairs at the mandible, eye lashes, skin coloration and fur. Scale bar: 5 cm for all stages (JPG 2032 KB)
429_2018_1725_MOESM3_ESM.jpg (1 mb)
Online resource 3. Body measures. We have plotted the body and organ weights and crown-rump-length. Measures have been taken during the final dissection. Every dot represents one animal, the average is the mean of the litter. The line connecting the litter average increases slowly at prenatal stages for most organs, but steeply after birth. The number of animals per litter is given in Table 1. Little information exists on fetal organ measures. Our values correspond with data reported for domestic pig (Mc-Phearson-McCassidy 2003) for liver (E45: 2g, E60: 4.5-9g), gastrointestinal tract (E60 2.5-4.6g; E75 14-20g), heart (E60: 0.7-0.9g; E102: 7-10g), lung (E60: 2.5-5.5g), and kidney (E60: 1.5-3g). (JPG 1057 KB)
429_2018_1725_MOESM4_ESM.jpg (1.7 mb)
Online resource 4 Variability of the sulcal pattern at E100. A: Dorsal view of brains of 5 sibling fetuses. The overall size of the brains is similar despite differences in body weights of the animals #1-#5 of 570g, 560g, 660g, 520g, and 390g, respectively. B: Outlines of the sulcal pattern with sulci encoded by color. Note the individual and left-right variability for instance for the cruciate sulcus in brain #5, or that the longest sulcus in the occipital region is usually the marginal sulcus, but could also be the endomarginal sulcus as in the right hemisphere of brain #3. The gray region is the representation of rostrum and face (Adrian 1943; Craner and Ray 1991). Abbreviations: see Fig. 1. Asterisk in brain no. 4: the spinal cord and cerebellum have been inadvertently sliced while opening the skull from the foramen magnum. In brains no. 2 and no. 3, cerebellum and brainstem had been removed before photographing. Scale bar: 2 cm for A, B. (JPG 1762 KB)
429_2018_1725_MOESM5_ESM.pptx (237 kb)
Online resource 5 Soma size development. A: Somata have been sampled in gray matter and marginal zone (GM/MZ), and B: Subplate and white matter (SP/WM). Size-frequency histograms (% per size bin [µm2]) reveal small somata at E60; SP/WM has too few NPY-ir neurons at this age to be analyzed separately. Soma size in GM/MZ remain small at E70 due to the presence of numerous immature neurons. Sizes of neurons in SP/WM are already larger. At E85, both compartments display much larger neurons and at E110 an adult size variation is present when compared to P30. Per age, 30-70 somata in gray matter and 50-80 somata in SP/WM have been analyzed in cryostat sections. (PPTX 236 KB)
429_2018_1725_MOESM6_ESM.pptx (1.9 mb)
Online resource 6 Cellular innervation pattern. A, B: GAD-65/67-ir neurons of the MZ have NPY-ir boutons in close apposition to somata and proximal dendrites. Note that the large NPY-ir boutons are GAD-negative. C, D: NPY-ir (red), GAD-negative neurons in CP/GM matter have GAD-65/67–ir (green) boutons in close apposition to somata and proximal dendrites. Arrows point to boutons. Scale bars: 10 µm. (PPTX 1995 KB)
429_2018_1725_MOESM7_ESM.jpg (3 mb)
Online resource 7 Pial blood vessel innervation. A, B: NPY-ir axons, single or in fascicles with coarse boutons occuring on pial vessels from E45 onwards. C, D: E60, E: E85; note that vessel innervation is much thicker than the varicose axons innervating the MZ. F, G: E100. H-J: P30; note in J that the coarse NPY-ir axons do not follow vessels that have penetrated into the cortex (pial surface is to the top). Scale bar: 20 µm for A-J. (JPG 3033 KB)
429_2018_1725_MOESM8_ESM.pptx (58 kb)
Online resource 8 Quantitative data on development of the AIS. Refers to Fig. 8I. A: Gap length between point of axon origin and begin of the βIV-spectrin-ir AIS in NPY-ir neurons in GM and WM. B: Length of the AIS of NPY-ir neurons in GM and WM. Number of AIS measured is indicated above the boxes; numbers for AIS length are smaller because the AIS was not always represented completely in the optical section. Gaps significantly shorten between E110 and P30, AIS length increases significantly between E85 and E110; Mann-Whitney U-test. C: AIS length of presumably mostly pyramidal neurons of supragranular layers are reported for comparison; their average length steadily increases from E85 to P30. (PPTX 58 KB)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Laura Ernst
    • 1
  • Simon Darschnik
    • 1
  • Johannes Roos
    • 2
  • Miriam González-Gómez
    • 3
  • Christa Beemelmans
    • 4
  • Christoph Beemelmans
    • 4
  • Maren Engelhardt
    • 2
  • Gundela Meyer
    • 5
  • Petra Wahle
    • 1
    Email author
  1. 1.Developmental Neurobiology, Faculty of Biology and BiotechnologyRuhr University BochumBochumGermany
  2. 2.Institute of Neuroanatomy, Medical Faculty Mannheim, CBTMHeidelberg UniversityHeidelbergGermany
  3. 3.Unit of Histology, Anatomy and Histology, Department of Basic Medical Science, Faculty of MedicineUniversity of La LagunaSanta Cruz de TenerifeSpain
  4. 4.Regionalverband Ruhr Grün, Forsthof Üfter MarkSchermbeckGermany
  5. 5.Unit of Histology, Department of Basic Medical Science, Faculty of MedicineUniversity of La LagunaSanta Cruz de TenerifeSpain

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