Three-dimensional Maxillary canal reconstruction of ancient mammal relative Cotylorhynchus romeri shows similarity to mammal sensory innervation

The trigeminal nerve is the fifth cranial nerve that provides both motor and sensory innervation to the face. There are three major branches of the trigeminal nerve: the ophthalmic, maxillary, and mandibular nerves. Here we focus on the evolution of the maxillary nerve (CN V2). In humans and mammals, the maxillary nerve transmits sensation from the maxilla, nasal cavity, sinuses, palate, and the mid-face. CN V2 is a highly branched structure whose branches travel through the pterygopalatine fossa and the infraorbital canal before branching into terminal nerves within soft tissue.

In ancient mammal relatives, the non-mammalian synapsids, the maxillary nerve travels through the maxillary canal. The maxillary canal is a bony tube that runs through the maxilla and the premaxilla parallel to the tooth row. Synapsids are a group of amniotes that first appeared 320 million years ago and include mammals and their ancient fossil relatives. The maxillary canal has been used as a phylogenetic character to distinguish fossils at the amniote split as either synapsids or diapsids, the group that likely includes all extant reptiles. The synapsid condition has been found to be a highly branched structure while the diapsid condition has been found to be a long singular tubular structure. The maxillary canal has been reconstructed in only two other very early diverging synapsids. The morphology of the maxillary canal in Caseidae, a group phylogenetically closer to the divergence of synapsids from the amniote common ancestor is not well-understood. To test whether these early-diverging synapsids shared a similar branched morphology with their later-diverging members of their clade or had a more diapsid-like condition, we reconstructed the maxillary canal of Cotylorhynchus romeri, a caseid synapsid from the ~280-million-year-old Lower Hennessey Formation of Oklahoma that is well known for its disproportionately small head compared to its large body.

We obtained computed tomography (CT) scans of a complete adult skull (OMNH 4329) and a partial juvenile skull (OMNH 4188). CT scanning allows us to view the internal structures of fossils without having to use any destructive methods. Using the CT scans, we manually segmented and reconstructed the maxillary canals using Avizo 2020.1.

In both OMNH 4329 and OMNH 4188, the maxillary canal displays a long structure that is highly branched, ramifying in multiple directions. This is similar to what has been described in other early diverging synapsids and their later diverging relatives, therapsids. We did not find any major ontogenetic differences between the two specimens, which was what we expected for cranial nerves, which are patterned early in development.

This highly branched maxillary canal in Cotylorhynchus romeri shows that it likely had extensive sensory facial innervation comparable to the later diverging non-mammalian synapsid relatives and even modern mammals. Because we found this highly branched morphology very close to the amniote split, this adds more evidence that this structure can be used as a phylogenetic character to help distinguish fossils as synapsids or diapsids.