Segmental Analysis of the Vestibular Nerve and the Efferents of the Vestibular Complex

Abstract

Use of a segmental approach in the study of vestibular centers in the hindbrain improves morphological and functional understanding of this region controlled by Hox genes, among other molecular determinants. Here, we review accrued data about segmental organization of vestibular afferents and efferents. Inner ear-originated vestibular fibers enter the hindbrain, together with auditory ones, through the alar plate of rhombomere 4, then branch into descending and ascending branches to reach appropriate vestibular nuclei along the vestibular column. Classical vestibular nuclei (superior, lateral, medial, and inferior) originate in eight successive rhombomeric segments, which suggests internal subdivisions correlated with distinct connections and functions. The vestibular projection neurons identified for various targets aggregate in discrete groups, which correlate topographically either with rhombomeric units, or with internal subdivisions within them. Each vestibular projection system (e.g., vestibulo-spinal, vestibulo-ocular, vestibulocerebellar) has a characteristic ipsilateral/contralateral organization. Comparing them as a connective mosaic in different species shows that various aspects of this segmental connective organization are conserved throughout evolution in vertebrates. Furthermore, certain genes that control the development of the rhombomeric units in the hindbrain may determine, among other aspects, the specific properties of the different neuronal subpopulations related to their axonal navigation and synaptogenesis. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc.

Axonal Projection Patterns of the Dorsal Interneuron Populations in the Embryonic Hindbrain

“…These different neuronal subtypes were found to depend on their rhombomeric origin; in r1, the most dorsal part of the RL contributes a large migratory cell population that forms the external and internal granular layers of the cerebellum (Ben-Arie et al, 1997;Wingate and Hatten, 1999;Köster and Fraser, 2001;Machold and Fishell, 2005). In r2-r6, the same RL domain generates auditory and vestibular nuclei, through which information is processed and relayed to the upper brain and spinal cord, whereas, in r6-r8, it will give rise to multiple pre-cerebellar nuclei which relay peripheral sensation to the cerebellum through mossy fiber neurons Bayer, 1980, 1987a,b,c,d;Rubel and Parks, 1988;Cambronero and Puelles, 2000;Rodriguez and Dymecki, 2000;Bermingham et al, 2001;Díaz et al, 2003;Ryugo and Parks, 2003;Pasqualetti et al, 2007;Hoshino et al, 2013;Kratochwil et al, 2017;Díaz and Puelles, 2019;Elliott et al, 2021). Similarly, different types of respiratory and viscerosensory nuclei are suggested to be born from more ventral positions of the RL at distinct axial levels, such as the parabrachial and Kölliker-Fuse nuclei that derive from r1, the A5 and intertrigeminal region that derives from r4-r6, the PreBötzinger complex and retrotrapezoid nucleus (RTN) that derive from r3/r5, and the nucleus tractus solitaries that is thought to derive from more posterior rhombomeres (Qian et al, 2001;Gray, 2008).…”

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 review analyzes how inner hair cells codify truly auditory messages, whereas the outer cells inform about mechanical aspects of the state of the organ of Corti. The second article examines the vestibular nerve and is focused on segmental analysis of afferents and efferents of the vestibular complex (Diaz and Puelles, ). Inner ear‐originated vestibular fibers enter through the alar plate of rhombomere 4 to reach the different components of the vestibular complex.…”