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

Abstract

Amphioxus is the living chordate closest to the ancestral form of vertebrates, and in a key position to reveal essential aspects of the evolution of the brain Bauplan of vertebrates. The dorsal neural cord of this species at the larval stage is characterized by a small cerebral vesicle at its anterior end and a large posterior region. The latter is comparable in some aspects to the hindbrain and spinal cord regions of vertebrates. The rostral end of the cerebral vesicle contains a median pigment spot and associated rows of photoreceptor and other nerve cells; this complex is known as "the frontal eye." However, this is not a complete eye in the sense that it has neither eye muscles nor lens (only a primitive retina-like tissue). Cranial nerves III, IV, and VI take part in the motor control of eye muscles in all vertebrates. Using a recent model that postulates distinct molecularly characterized hypothalamo-prethalamic and mesodiencephalic domains in the early cerebral vesicle of amphioxus, we analyze here possible scenarios for the origin from the common ancestor of cephalochordates and vertebrates of the cranial nerves related with extrinsic eye muscle innervations. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc.

Is There a Prechordal Region and an Acroterminal Domain in Amphioxus?

“…With the beginning of gene expression studies at the end of the twentieth century, it was suggested again that the CNS of vertebrates is homologous to the entire CNS of amphioxus [Holland et al, 1992;Lacalli et al, 1994;Lacalli, 1996]. However, only recently were details of potential topologic and molecular regional correspondence of the brain Bauplan of amphioxus versus that of vertebrates examined in terms of specific rostrocaudal neuromeric or DV longitudinal divisions and gene patterns [Albuixech-Crespo et al, 2017;Ferran and Puelles, 2019]. According to this genoarchitectonic analysis, the brain vesicle of the amphioxus neurula reveals at its rostral end three molecularly distinct neuromeric units forming an AP series along the rostrocaudal dimension.…”

Cranial Nerves: Mind Your Head

“…This Special Issue of The Anatomical Record compiles works in the above mentioned Ontogeny/Phylogeny and Morphology/Clinical Significance topics. The organizational/developmental point of view (Volume 1 of this Special Issue) is populated with the long debated cranial par 0 or nervus terminalis (Peña‐Melián et al ., ), the very atypical and interesting features of the olfactory nerve (Crespo et al ., ), the development and pathologies of optic nerves (Herrera et al ., ), the organization and function of the oculomotor complex in different vertebrate brains, and the complex evolutionary relationships derived from the comparative analysis of eye muscles innervation (Company et al ., ; Ferran and Puelles, ), the anatomy and physiology of the auditory portion of the VIIIth nerve and the segmental organization of vestibular complex afferents and efferents (Carricondo and Romero‐Gómez, ; Diaz and Puelles, ), the atypical features of the spinal accesory motor neurons and the present neuromeric brainstem conception (prosomeric model) after new data from the visceral cranial nerve efferents (Puelles et al ., ; Watson and Tvrdik, ), and characterization of the cranial nerves in lampreys (Pombal and Megías, ). This volume 1 Ontogeny/Phylogeny of the Cranial Nerves Special Issue is completed with a historical overview of the cranial nerves (Porras et al ., ).…”

Cranial Nerves: Phylogeny and Ontogeny

“…The phylogeny and ontogeny volume includes an historical review (Porras‐Gallo et al, ), a review from a segmental perspective (Puelles et al, ), two comparative contributions on amphioxi (Ferran and Puelles, ) and lampreys (Pombal and Megías, ), and articles devoted to cranial nerves zero (Peña‐Melián et al, ), I (Crespo et al, ), II (Herrera et al, ), III, IV and VI (Company et al, ), VIII cochlear (Carricondo and Romero‐Gómez, ) and vestibular (Diaz and Puelles, ), and XI (Watson and Tvrdik, ).…”

“…This is followed by an article on the organization of the oculomotor complex in amphioxi, which is reviewed from a comparative perspective (Ferran and Puelles, ). Amphioxi are the living chordates closest to the ancestral vertebrate, and are key to understanding the vertebrate brain bauplan.…”