Restoration of the Topological Organization of the Trigeminal System Following Trigeminal Nerve Root Injury in the Lamprey

• Published in: Neuroscience 2019-12, Vol.423, p.216-231
• Main Authors: Ly, Lexie T., Benthall, Katelyn N., Pale, Timothee, McClellan, Andrew D.
• Format: Article
• Language: English
• Subjects: cranial nerves; regeneration; somatotopic; topographical; trigeminal
• ISSN: 0306-4522; 1873-7544
• DOI: 10.1016/j.neuroscience.2019.08.044

[Display omitted] •Trigeminal motor and sensory divisions in the lamprey are topologically organized.•Motor topological organization is restored following trigeminal nerve transection.•Sensory topological organization is poorly restored following nerve injury.•However, trigeminal sensory-evoked responses recover following injury.•Several factors probably contribute to the restoration of topological organization. Two issues were examined regarding the trigeminal system in larval lampreys: (1) for normal animals, double labeling was used to confirm that the trigeminal system has a topological organization; (2) following trigeminal nerve root transections, double labeling was used to test whether the topological organization of the trigeminal system is restored. First, for normal animals, Alexa 488 dextran amine applied to the medial oral hood (anterior head) labeled trigeminal motoneurons (MNs) in the ventromedial part of the trigeminal motor nuclei (nVm) and axons of trigeminal sensory neurons (SNs) in the ventromedial part of the trigeminal descending tracts (dV). Also, Texas red dextran amine (TRDA) applied to the lateral oral hood labeled trigeminal MNs in the dorsolateral nVm and sensory axons in the dorsolateral dV. These results confirm the topological organization of the trigeminal system of normal lampreys. Second, following trigeminal nerve root transections, the physical integrity of the nerves was restored during growth of trigeminal sensory and motor axons. In addition, double labeling indicated a restoration and refinement of the topological organization of the trigeminal system with increasing recovery times, but mainly for nVm. Despite the paucity of growth of trigeminal sensory axons in dV even at long recovery times (12–16 wks), a substantial percentage of experimental animals recovered trigeminal-evoked swimming responses and trigeminal-evoked synaptic responses in reticulospinal (RS) neurons. Following trigeminal nerve root injury, several mechanisms, including axonal guidance cues, probably contribute to the substantial restoration of the topological organization of the lamprey trigeminal system.