A hindbrain segmental scaffold specifying neuronal location in the adult goldfish, Carassius auratus

Abstract

The vertebrate hindbrain develops as a series of well-defined neuroepithelial segments or rhombomeres. While rhombomeres are visible in all vertebrate embryos, generally there is not any visible segmental anatomy in the brains of adults. Teleost fish are exceptional in retaining a rhombomeric pattern of reticulospinal neurons through embryonic, larval, and adult periods. We use this feature to map more precisely the segmental imprint in the reticular and motor basal hindbrain of adult goldfish. Analysis of serial sections cut in three planes and computer reconstructions of retrogradely labeled reticulospinal neurons yielded a segmental framework compatible with previous reports and more amenable to correlation with surrounding neuronal features. Cranial nerve motoneurons and octavolateral efferent neurons were aligned to the reticulospinal scaffold by mapping neurons immunopositive for choline acetyltransferase or retrogradely labeled from cranial nerve roots. The mapping corresponded well with the known ontogeny of these neurons and helps confirm the segmental territories defined by reticulospinal anatomy. Because both the reticulospinal and the motoneuronal segmental patterns persist in the hindbrain of adult goldfish, we hypothesize that a permanent "hindbrain framework" may be a general property that is retained in adult vertebrates. The establishment of a relationship between individual segments and neuronal phenotypes provides a convenient method for future studies that combine form, physiology, and function in adult vertebrates.

Ontogenetic Development of Vestibulo-Ocular Reflexes in Amphibians

“…In contrast to the midbrain origin of oculomotor motoneurons, trochlear and abducens motoneurons in anurans originate from rostral r1 and from r5, respectively (Straka et al, 1998, 2006). The mono-segmental origin of the latter nucleus is similar to that reported for mammals but differs from the bi-segmental pattern of fish and birds, where abducens motoneurons derive from both r5 and r6 (see Straka et al, 2006; Gilland et al, 2014). In addition, abducens internuclear neurons with crossed ascending projections to contralateral MR motoneurons in the oculomotor nucleus are intermingled with abducens motoneurons in r5 (Straka and Dieringer, 1991; Straka et al, 2001).…”

Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective

“…Shared efferent neurons, with an origin in r4 project to all inner ear endorgans as well as to neuromasts supplied by the aLLN [Chagnaud et al 2015; Hellmann and Fritzsch 1996]. In contrast, a second set of efferent neurons, which derives from r6 project to those neuromasts along the body that are innervated by the pLLN [Chagnaud et al 2015; Gilland et al 2014]. Despite the common origin, the functional consequence of efferent activation differs between the vestibular and lateral line system.…”

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

“…Anteroposteriorly, the embryonic hindbrain shows a number of overt (visibly delimited) rhombomeres (this is the generic name given to transverse neuromeres or segments in the hindbrain), as well as a set of hidden (cryptic, that is, morphologically non‐distinct, but nevertheless molecularly bounded) rhombomeres, the latter being known as cryptorhombomeres. In mammals and birds (probably in all vertebrates) there is a total of 12 hindbrain rhombomeres (r0‐r11) (Watson et al, ; Puelles, ; Puelles et al, ; Gilland et al, ; Tomás‐Roca et al, ; Watson et al, ,b,c), of which r2‐r6 are overt (forming distinct transverse bulges at early stages), and r0‐r1 plus r7‐r11 are cryptic (not visibly delimited; r0 corresponds to the classic isthmus) (Watson et al, ). The r0‐r2 units are topographically prepontine, while the basilar pons occupies r3‐r4; the retropontine r5‐r6 units are often wrongly ascribed to the pons in the human brainstem, because the massively bulging pons overhangs them ventrally; finally, the r7‐r11 units build up the medulla oblongata; the rhombo‐spinal boundary lies precisely above the pyramidal decussation, coinciding with the center of the 5th somite.…”

“…As regards the efferent neurons of cranial nerves, they are located according to a rhombomeric organization in all studied vertebrates (Gilland and Baker, ; Gilland et al, ). In most vertebrates the efferent neurons of the eighth nerve originate in the basal plate of r4, and their axons exit with the vestibular root (auditory efferents pass extraneurally to the auditory root).…”