Vestibular Blueprint in Early Vertebrates
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REVIEW ARTICLE published: 19 November 2013 doi: 10.3389/fncir.2013.00182 Vestibular blueprint in early vertebrates Hans Straka 1* and Robert Baker 2 1 Department Biology II, Ludwig-Maximilians-Universität München, Planegg, Germany 2 Department of Neuroscience and Physiology, Langone Medical Center, New York University, New York, NY, USA Edited by: Central vestibular neurons form identifiable subgroups within the boundaries of classically Catherine Carr, University of outlined octavolateral nuclei in primitive vertebrates that are distinct from those processing Maryland, USA lateral line, electrosensory, and auditory signals. Each vestibular subgroup exhibits Reviewed by: a particular morpho-physiological property that receives origin-specific sensory inputs Leonard Maler, University of Ottawa, Canada from semicircular canal and otolith organs. Behaviorally characterized phenotypes send Joel C. Glover, University of Oslo, discrete axonal projections to extraocular, spinal, and cerebellar targets including other Norway ipsi- and contralateral vestibular nuclei. The anatomical locations of vestibuloocular and *Correspondence: vestibulospinal neurons correlate with genetically defined hindbrain compartments that are Hans Straka, Department Biology II, well conserved throughout vertebrate evolution though some variability exists in fossil and Ludwig-Maximilians-Universität München, Grosshadernerstr. 2, 82152 extant vertebrate species.The different vestibular subgroups exhibit a robust sensorimotor Planegg, Germany signal processing complemented with a high degree of vestibular and visual adaptive e-mail: [email protected] plasticity. Keywords: semicircular canal, otolith, eye movements, extraocular motoneurons, goldfish, hindbrain segment, vestibuloocular, vestibulospinal INTRODUCTION contain a crista covered by a gelatinous cupula that is deformed by In the best-studied early vertebrates that largely represent fish fluid motion during rotational movements of the head/body, thus species, particularly goldfish (Carassius auratus), the octavolateral acting as force transducers of angular acceleration. By contrast, nuclei occupy a considerable part of the dorso-lateral hind- the utricle is filled with movable carbonate stones overlying fixed brain between the fifth and tenth cranial nerves (Figures 1A,B). hair cells and is highly effective for transducing linear accelera- Functionally, the octavolateral nuclei are heterogeneous sub- tion. The major role of the utricle in all vertebrates is for sensing groups of neurons subserving four different sensory modalities: inertia through detection of static changes in head/body posi- lateral line for detection of either water motion (mechanorecep- tion relative to the earth gravitation vector thereby creating an tive) or objects (electroreceptive), auditory for acoustic pressure internal“frame of reference”for orientation and locomotor behav- and vestibular for body motion (McCormick, 1983; Mered- iors (Baker, 1998; Hess and Angelaki, 1999). Vestibular afferent ith, 1988; Highstein et al., 1992; McCormick and Braford, fibers are segregated from all other eighth nerve components and 1994; Straka and Baker, 2011; McCormick and Wallace, 2012). project to the most lateral neuronal subgroups in the hindbrain The peripherally located epithelial endorgans for these four (Figures 2A,B). Based on their evolutionary-conserved neuronal sensory modalities develop from a common placodal region projections to brainstem and spinal regions responsible for the and the sensory transduction mechanism is largely based control of balance and locomotion, the lateral portions of the on the same ancestral hair cell-type receptor (Fritzsch et al., octavolateral nuclei can be clearly distinguished from the more 2002; Modrell et al., 2011). This ubiquitous mechanoreceptor- medial, and dorsal nuclei that process acoustic and lateral line type cell is used to detect and convert respective physical sensory signals (Figures 2A,B). forces into neuronal activity clearly distinguishing between electro- and mechano-sensory stimuli. Peripheral octavolat- HINDBRAIN SEGMENTAL ORGANIZATION OF VESTIBULAR eral hair cells are linked to first order afferent nerve fibers SUBGROUPS from either the lateral line/electrosensory neuromasts on the The most comprehensive developmental and topographical map- body surface or specialized vestibular/auditory endorgans to ping of overall vestibular organization has been carried out in distinct nuclear regions in the dorsal hindbrain (McCormick cyprinids (goldfish and zebrafish). Based on the cellular organiza- and Braford, 1994; McCormick and Hernandez, 1996; tion, the vestibular nuclei are generally illustrated as five major Straka and Baker, 2011). subdivisions of second order neurons related to balance, pos- Vestibular sensory function in the somewhat inappropriately tural control, and motion (Figure 1B). Each subdivision can called “inner ear” of early vertebrates consists of separate semi- be further divided into distinct functional groups involved in circular canals attached to a single sac-like structure, the utricle the control of eye and body motion based on (1) regionally with additional sac-like structures, the saccule, and the lagena, restricted terminations of first order afferent fibers from the differ- utilized for audition and/or graviception (Fritzsch et al., 2002) ent peripheral vestibular endorgans, (2) anatomical tract tracing and magnetoreception (Wu and Dickman, 2012). The semicircu- from efferent projection areas in the midbrain, hindbrain and lar canals are oriented at right angles from each other comprising spinal cord (SC), and (3) electrophysiological correlates of second different planes. Expansions in each canal known as ampullae order neurons during different behavioral paradigms (Highstein Frontiers in Neural Circuits www.frontiersin.org November 2013 | Volume 7 | Article 182 | 1 “fncir-07-00182” — 2013/11/18 — 17:41 — page1—#1 Straka and Baker Archetypical vestibular organization FIGURE 1 | Location of the octavolateral vestibular subdivisions within FIGURE 2 | Afferent and efferent vestibular pathways in adult goldfish. the goldfish hindbrain. A side view of the intact brain (A) and sagittal Schematic cross sections at the level of r3 (A) and r5 (B) showing first schematic diagram (B) are drawn at the same scale. Vertical dashed lines order canal and utricular afferent terminations. Efferent projections to ipsi- indicate rostro-caudal levels of the coronal sections shown in Figure 2.AO, and contralateral extraocular, spinal, cerebellar, and vestibular targets are DO, MO, PO, anterior, descending medial, posterior octavolateral nuclei; color-coded. Reconstruction based on own data (Straka and Baker, CC, corpus cerebelli; Egr, external granule cell layer; FL, facial lobe; gr, unpublished) and published material (McCormick and Braford, 1994). AI, corpus cerebelli granule cell layer; HYP,hypothalamus; III, IV, and VI abducens internuclear neurons; ABD, abducens motoneurons; AO, DO, oculomotor, trochlear, and abducens nuclei; VIIIn, IXn Xn, and Vn, vestibular, anterior, descending octavolateral nucleus; CC, cerebellar crest; EG, glossopharyngeal, vagal, and trigeminal nerves; IO, inferior olive; LC, lobus eminentia granularis; LC, caudal lobe; MAN, medial auditory nucleus; MED, caudalis; ML, molecular layer of crus cerebelli; VC, valvula cerebelli; OT, lateral line medial nucleus; MLF,medial longitudinal fasciclus; T, tangential optic tectum; SC, spinal cord; T, tangential nucleus; VAG, vagal lobe. nucleus; GTr, secondary gustatory tract; PllTr, posterior lateral line tract; VTr, descending tract of the Vth cranial nerve; VIITr, central tract of the seventh cranial nerve. et al., 1992; McCormick and Braford, 1994; McCormick and Her- nandez, 1996; Graf et al., 2002; McCormick and Wallace, 2012). each vestibular functional phenotype. This genetic and compart- The structural and functional similarity of the major vestibular cell mental blueprint appears to be shared between all species of fish. groups across different fish species allows vestibuloocular, vestibu- Based on knowledge of neuronal position within the embryonic lospinal, vestibulocommissural, and vestibulocerebellar neurons hindbrain, it is therefore possible to recognize the ontogenetic ori- to be identified as distinct populations (Figures 2A,B). gin of each vestibular subnucleus in adult fish with respect to the All vestibular subgroups develop within a hindbrain segmen- underlying hindbrain segmental scaffold and to link it with the tal framework that consists of eight well-defined neuroepithelial adult architecture of the various vestibular subdivisions (Baker, segments, rhombomeres (r) 1-8 (Figure 3; Vaage, 1969; Gilland 1998; Fritzsch, 1998). and Baker, 1993; Straka et al., 2001; Gilland and Baker, 2005). The vestibular column originates largely from embryonic compart- EVOLUTION OF VESTIBULAR SUBGROUPS ments r2-7, and thus spans nearly the entire rostro-caudal extent of Vestibular neuronal subgroups evolved long before fishes in the the hindbrain (Figure 3). Distinct subsets of vestibuloocular neu- earliest jawless vertebrates as, e.g., lamprey (Figure 4; Gilland rons in r1-3 and r5-6 and of vestibulospinal neurons in r4-6 occupy and Baker, 1993; Pombal et al., 1996; Baker, 1998). Interestingly, unique segmental compartments, respectively (Figures 3–5). Each lampreys have only two semicircular canals, the anterior (AC), hindbrain segment is characterized by a combinatorial expression and posterior vertical canal (PC), that contribute