Anat Cell Biol.  2019 Sep;52(3):278-285. 10.5115/acb.19.020.

Nervus terminalis and nerves to the vomeronasal organ: a study using human fetal specimens

• Jin ZW
• Cho KH
• Shibata S
• Yamamoto M
• Murakami G
• Rodríguez-Vázquez JF

• KMID: 2459543
• DOI: http://doi.org/10.5115/acb.19.020

Abstract

The human nervus terminalis (terminal nerve) and the nerves to the vomeronasal organ (VNON) are both associated with the olfactory nerves and are of major interest to embryologists. However, there is still limited knowledge on their topographical anatomy in the nasal septum and on the number and distribution of ganglion cells along and near the cribriform plate of the ethmoid bone. We observed serial or semiserial sections of 30 fetuses at 7-18 weeks (crown rump length [CRL], 25-160 mm). Calretinin and S100 protein staining demonstrated not only the terminal nerve along the anterior edge of the perpendicular lamina of the ethmoid, but also the VNON along the posterior edge of the lamina. The terminal nerve was composed of 1-2 nerve bundles that passed through the anterior end of the cribriform plate, whereas the VNON consisted of 2-3 bundles behind the olfactory nerves. The terminal nerve ran along and crossed the posterior side of the nasal branch of the anterior ethmoidal nerve. Multiple clusters of small ganglion cells were found on the lateral surfaces of the ethmoid's crista galli, which are likely the origin of both the terminal nerve and VNON. The ganglions along the crista galli were ball-like and 15-20 µm in diameter and, ranged from 40-153 in unilateral number according to our counting at 21-µm-interval except for one specimen (480 neurons; CRL, 137 mm). An effect of nerve degeneration with increasing age seemed to be masked by a remarkable individual difference.

Keyword

Nervus terminalis; Vomeronasal organ; Olfactory nerve; Calretinin; Human embryo

MeSH Terms

Calbindin 2
Ethmoid Bone
Fetus
Ganglion Cysts
Humans*
Individuality
Masks
Nasal Septum
Nerve Degeneration
Neurons
Olfactory Nerve
Vomeronasal Organ*

Figure

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  Fig. 1 The terminal nerve and nerves to the vomeronasal organ (VNON) are closely located in a specimen of crown rump length 45 mm (9 weeks). Sagittal sections. Immunohistochemistry of S100 protein (S100) (A, D, E) or calretinin (cal) (B, C, F, G). Panels A and D display the lateral planes in the figure, while panels B, C, F, and G display the medial planes. Thus, the upper or lower raw of panels exhibits a different side from the lateral to the medial, respectively. Intervals between panels are 0.2 mm (A–B), 0.1 mm (B–C), 0.2 mm (D–E), and 0.1 mm (E–F, F–G). On one side (panels A–C), the proximal course of the VNON was not cut, and we did not identify the distal course of the terminal nerve (NT) on the other side (panels D–G). Open stars in panels E and F indicate the most likely candidate of the terminal nerve. Arrowhead in panel D indicates an on-going fusion between the nasal septum and palate. In the specimen, the terminal nerve and VNON appeared to be closely located in the nasal septum. VNO, vomeronasal organ. Scale bars=1 mm (A–G).

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  Fig. 2 The terminal nerve and nerves to the vomeronasal organ (VNON) are separated by a developing nasal septum in a specimen of crown rump length 110 mm (15 weeks). Sagittal sections. Immunohistochemistry of S100 protein (S100) (A, C) or calretinin (cal) (D). (B) Hematoxylin and eosin staining. Panels C and D display the vomeronasal organ (VNO) and VNON in the other side of panels A and B. Intervals between panels are 0.2 mm (A–B), 0.6 mm (B–C), and 0.1 mm (C–D). In panel A, the terminal nerve (NT) runs along the posterior aspect of the cartilaginous nasal bone, while the VNON run along the palate near the VNO. Thus, these nerves are separated by a developing nasal septum. Scale bars=1 mm (A–D).

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  Fig. 3 Anterior ethmoidal nerve coming from the orbit in a specimen of crown rump length 27 mm (7 weeks). Sagittal sections. Hematoxylin and eosin staining. Panel A (or F) displays the most lateral (or medial) plane in the figure. Intervals between panels are 0.3 mm (A–B, B–C), 0.05 mm (C–D, D–E), and 0.1 mm (E–F). The anterior ethmoidal nerve (AEN) runs medially from the orbit (A–C), reaches the superolateral angle of the nasal cavity (D), and directs inferiorly along the mucosal membrane (E, F). Panels A–D were prepared at the same magnification (scale bar in panel A=1 mm). FN, frontal nerve; MC, Meckel's cartilage; OCN, oculomotor nerve; PPG, pterygopalatine ganglion; TG, trigeminal nerve ganglion.

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  Fig. 4 Anterior ethmoidal nerve crossing superficially the terminal nerve in a specimen of crown rump length 27 mm (7 weeks). Sagittal sections. Hematoxylin and eosin staining. Panels A and F display the lateral sites, while panels B and C show planes near the midsagittal plane. Thus, the terminal nerve (NT) is seen bilaterally (A, D). Panel F is 0.2 mm medial to Fig. 3F. Panel E is the higher magnification view of a square in panel D. Intervals between panels are 0.2 mm (A–B), 0.1 mm (B–C, C–D, D–F). The terminal nerve appears to be still closely related to the nerves to the vomeronasal organ (VNON) candidate (VNON? in panel B). In the immediately superior side of the cartilaginous nasal bone, the anterior ethmoidal nerve (AEN) crosses superficially the terminal nerve without communication (E, F). Panels A–D were prepared at the same magnification. Scale bars=1 mm (A), 0.1 mm (E, F).

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  Fig. 5 Ganglion cells on the lateral surface of the crista galli of the ethmoid in a specimen of crown rump length 160 mm (18 weeks). Frontal sections. Panel A is 2.0 mm anterior to panel D. Panel B (or C) is a higher magnification view of a square in panel A (or B). Panel E is a higher magnification view of a square in panel D. Panel F is a section near panel E. Hematoxylin and eosin staining (A, F) or immunohistochemistry of neuron specific enolase (NSE) (B, C) and S100 protein (S100) (D, E). Ganglion cells on the crista galli are, 15–20 µm in diameter, positive for NSE (arrows in panels C), negative for S100 (arrows in panel E), and highly eosinophilic (arrows in panel F). Scale bars=1 mm (A, B, D), 0.1 mm (C, E, F). NS, nasal septum.

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