Segmental arrangement of reticulospinal neurons in the goldfish hindbrain

Abstract

The hindbrain is evolutionarily conserved among diverse vertebrate phyla. In vertebrate embryos, the hindbrain is segmentally organized as a series of overt swellings known as rhombomeres. In the larval zebrafish Brachydanio rerio, conspicuous and identifiable reticulospinal neurons are positioned in the center of rhombomeres. Segmentally homologous reticulospinal neurons that share a range of morphological, developmental, and biochemical features occupy adjacent rhombomeres. We have recently shown that reticulospinal neurons of the zebrafish survive ontogeny without considerable morphological modification and we suggested that homologous neurons may share similar functions at different stages of development (Lee and Eaton: Journal of Comparative Neurology 304:34-52, 1991). The goldfish Carassius auratus, a related cyprinid, is especially suited for neurophysiological and behavioral studies. However, it is not yet known if the various reticulospinal neurons of zebrafish are generalizable to other species such as the goldfish. Therefore, we sought to examine the extent to which reticulospinal neurons of the zebrafish are also present in the adult goldfish. Analysis of 45 brains retrogradely labeled with horseradish peroxidase (HRP) from the spinal cord showed that reticulospinal neurons are arranged as a series of seven segments within the hindbrain; a regular interval of approximately 200 microns separates adjacent segments. Although the goldfish reticulospinal system has more neurons than the zebrafish, many reticulospinal neuron types continue to be identifiable. Moreover, comparisons of dendritic arborizations and axon paths between the two species showed that the morphology between various neuron types is virtually identical. The cross-taxonomic similarities between the reticulospinal systems of these related cyprinids make it possible to pursue functional considerations of segmentally homologous neurons in the goldfish hindbrain.

Common Sensory Inputs and Differential Excitability of Segmentally Homologous Reticulospinal Neurons in the Hindbrain

“…In this study, ϳ90% of the recorded neurons were successfully labeled with neurobiotin iontophoretically injected through the recoding micropipette. Four types of RS neurons (MiD-cm, MiD-cl, MiD-i, and MiV) were identified in r5 and r6, as shown previously (Metcalfe et al, 1986;Lee et al, 1993a). Among them, the RS neurons with axons that crossed the midline and descended along with the M-cell axon in the medial longitudinal fasciculus (mlf) toward the contralateral spinal cord were identified as MiD2cm or MiD3cm.…”

“…Hindbrain RS neurons were retrogradely labeled to investigate their rostrocaudal arrangement in adult goldfish, as shown previously in juvenile goldfish (Lee et al, 1993a). Fish were anesthetized with MS222 and mounted on the chamber as mentioned above.…”

“…1 A1), as described previously in juveniles (Lee et al, 1993a). By convention, these clusters are designated r1-r7 from rostral to caudal.…”

“…Seven clusters of reticulospinal (RS) neurons are periodically arranged along the neuraxis in the hindbrain of zebrafish and goldfish (Kimmel et al, 1982;Metcalfe et al, 1986;Lee and Eaton, 1991;Lee et al, 1993a) (see Fig. 1 A1).…”

Segmental development of reticulospinal and branchiomotor neurons in lamprey: insights into the evolution of the vertebrate hindbrain

“…In avians and teleosts, rhombomeres initially generate similar repeated sets of neurons belonging to distinct classes (Metcalfe et al, 1986;Mendelson, 1986a;Mendelson, 1986b;Kimmel et al, 1988;Lee et al, 1993;Hanneman et al, 1988;Kimmel, 1993;Clarke and Lumsden, 1993). Thus, each rhombomere seems to represent in its composition a serial homologue of a repeated repertoire of reticular neurons.…”