Gaskell revisited: new insights into spinal autonomics necessitate a revised motor neuron nomenclature

Abstract

Several concepts developed in the 19th century have formed the basis of much of our neuroanatomical teaching today. Not all of these were based on solid evidence nor have withstood the test of time. Recent evidence on the evolution and development of the autonomic nervous system, combined with molecular insights into the development and diversification of motor neurons, challenges some of the ideas held for over 100 years about the organization of autonomic motor outflow. This review provides an overview of the original ideas and quality of supporting data and contrasts this with more accurate and in depth insight provided by studies using modern techniques. Several lines of data demonstrate that branchial motor neurons are a distinct motor neuron population within the vertebrate brainstem, from which parasympathetic visceral motor neurons of the brainstem evolved. The lack of an autonomic nervous system in jawless vertebrates implies that spinal visceral motor neurons evolved out of spinal somatic motor neurons. Consistent with the evolutionary origin of brainstem parasympathetic motor neurons out of branchial motor neurons and spinal sympathetic motor neurons out of spinal motor neurons is the recent revision of the organization of the autonomic nervous system into a cranial parasympathetic and a spinal sympathetic division (that is, there is no sacral parasympathetic division). We propose a new nomenclature that takes all of these new insights into account and avoids the conceptual misunderstandings and incorrect interpretation of limited and technically inferior data inherent in the old nomenclature.

The Postmigratory Alar Topography of Visceral Cranial Nerve Efferents Challenges the Classical Model of Hindbrain Columns

“…Note that efferent ‘sympathetic preganglionic neurons’ also are produced in the ventral horn of thoracic and high lumbar levels, though they later translocate their somata via tangential migration into the lateral horn area, which plausibly develops in the neighboring liminal alar plate (Levi‐Montalcini, ; Yip et al, ; compare Ju et al, ; Puelles, ). The sacral spinal cord is widely held to produce in its basal plate some efferent parasympathetic preganglionic neurons, whose adult topography suggests that they imitate the basal–alar migratory behavior of thoracic sympathetic preganglionic elements (interestingly, a recent report doubts their parasympathetic nature; Fritzsch et al, ).…”

“…The second or pMNs‐like hindbrain basal microzone notably expresses Nkx6.1/6.2 transcription factors, whose effects in the presence of Pax6 and Olig2 signals lead to the production of somatomotor motoneurons (sm) at specific AP levels (r0 for the IVn; r5 in mouse or r5–r6 in sauropsids for the VIn; r8–r11 for the XIIn; Dubreuil et al, ; Pattyn et al, ). Analogous sm cells are formed at the midbrain m1 mesomere (IIIn) (note Fritzsch et al argue that III and IV efferent neurons represent a separate typological subgroup of vm cells, rather than somatomotor ones). The axons of the isthmic IV nerve are strongly repelled by signals diffusing from the isthmic floor plate sector, and thus select an alternative dorsalward route, which leads them to exit via a crossed root at the roof of the isthmus.…”

Lessons from Amphioxus Bauplan About Origin of Cranial Nerves of Vertebrates That Innervates Extrinsic Eye Muscles

“…; Marshall, ; Neal, ; Holland et al, ). These muscles are present in practically all vertebrates (lampreys and gnathostomes); but absent in hagfish (Fritzsch et al, ). However, prechordal plate cells were proposed to be the source of the premandibular lateral mesenchyme in vertebrates, whose derivatives are innervated by the III cranial nerve (Wachtler et al, ; Kuratani et al, ; Kuratani and Adachi, ).…”

“…Corroboration that the isthmus may be understood as a cryptorhombomere was provided recently by Watson et al () using analysis of Fgf8 ‐labeled progeny in a transgenic mouse line. In Wnt1 –/– mutants IsO development is affected, determining the absence of oculomotor (III) and trochlear nerves (IV); that might be linked to a Phox2 downregulation (Fritzsch et al, ). The origin and development of III and IV nuclei and roots in vertebrates is thus closely related with the evolutionary emergence of IsO activity, which lies upstream of the formation and identity specification of the mesencephalon (III par) and rhombomere 0 (IV par).…”

The emerging role of cranial nerves in shaping craniofacial development

“…This reflects the uniqueness of these motor neurons from other SM neurons due to their dependence on the transcription factor PHOX2A and lack of expression of other SM neuron‐specific transcription factors. The reader is referred to an excellent review discussing the most recent understanding of the molecular induction of motor neurons, which forms the basis for the suggested changes in nomenclature (Fritzsch, Elliott, & Glover, ).…”