Segmental homologies among reticulospinal neurons in the hindbrain of the zebrafish larva

Abstract

We have examined the morphology of identified reticulospinal neurons in larval zebrafish by retrogradely labeling them with horseradish peroxidase. We described the morphology of 27 different types of reticulospinal neurons found in the hindbrain 5 days after fertilization. Nineteen of these types are present as single identified neurons on each side of the brain; the others are present as pairs or small groups of cells. The hindbrain reticulospinal neurons are present in seven bilateral clusters that are spaced periodically along the neuraxis. Each cluster contains two to five different types of reticulospinal neurons. Cells with similar morphological features are found in adjacent clusters. By considering cell position within the cluster and axon pathway, nearly all of the cells can be assigned to one of about seven serially repeated classes. Independent morphological features of the cells support the same classification. We propose that the clusters represent hindbrain segments and that the neurons of the same class that are present in the different clusters are segmental homologues. Assuming that this series evolved by successive duplications and divergence of the primitive segments, we have analyzed the changes that may have occurred during the evolution of each new segment. Changes between ipsilaterally and contralaterally projecting axons may have occurred several times during the evolution of the series. In addition, cells may have been added or deleted.

Constructing the hindbrain: Insights from the zebrafish

“…This principle is also well illustrated by the zebrafish reticulospinal neurons, which lie laterally in even-numbered rhombomeres and more medially in odd-numbered rhombomeres ( Fig. 3A; Mendelson, 1986a,b;Metcalfe et al, 1986). In the chick, several lines of evidence point toward a two-segment periodicity within the hindbrain: the branchiomotor nerves that innervate the pharyngeal arches exit the hindbrain from even-numbered rhombomeres (Lumsden and Keynes, 1989); the timing of neuronal differentiation is delayed in odd-numbered rhombomeres (Lumsden and Keynes, 1989); cranial neural crest cells that contribute to the pharyngeal arches migrate from evennumbered rhombomeres ; and, finally, even-and odd-numbered rhombomeres exhibit different cell adhesive properties (Guthrie and Lumsden, 1991;Guthrie et al, 1993;Wizenmann and Lumsden, 1997).…”

“…The reticulospinal neurons differentiate early during hindbrain development in a reiterated pattern that persists long after the morphological segmentation of the hindbrain has become obscured ( Fig. 3A; Metcalfe et al, 1986;Mendelson, 1986a;Hanneman et al, 1988). Motor neurons, commissural neurons, and other, laterdifferentiating neuronal types also conform to this segmental pattern (Fig.…”

Control of visually guided behavior by distinct populations of spinal projection neurons

“…This image was passed through image segmentation filters in Matlab (Mathworks) to extract the volume occupied by each cell. Cell identities were assigned by hand on the basis of morphological criteria 13 . Cells with an evoked response greater than 0.1 Δf/f to at least one stimulus direction were assigned directionality vectors and a directional preference index (DPI) calculated as in a previous study 27 .…”

Visualization of two distinct classes of neurons by gad2 and zic1 promoter/enhancer elements in the dorsal hindbrain of developing zebrafish reveals neuronal connectivity related to the auditory and lateral line systems

“…By comparison with the positions of the reticulospinal neurons retrogradely labeled with tetramethylrhodamine-dextran (Metcalfe et al, 1986), we found that the majority of commissural fascicles were distributed from rhombomere (r)2 to r6 and that the caudal end of the longitudinal fascicle corresponded approximately to the caudal r6 border (Fig. 4C).…”