Neuronal adaptation accompanying metamorphosis in the flatfish.

Flatfish provide a natural paradigm to investigate adaptive changes in the central nervous system of vertebrates. During their metamorphosis, the animals undergo a 90 degrees tilt to one side or the other to become the bottom-adapted adult flatfish. The eye on the down side is pushed over to the up side. Thus, vestibular and oculomotor coordinate systems rotate 90 degrees relative to each other. As a result, during swimming movements different types of compensatory eye movements are produced before and after metamorphosis by the same vestibular stimulation. Intracellular staining of central neurons with horseradish peroxidase revealed that in postmetamorphic flatfish second-order horizontal canal neurons contact vertical eye muscle motoneuron pools on both sides of the brain via pathways that are absent in all other vertebrates studied. These unique connections provide the necessary and sufficient connectivity to adapt the flatfish's eye movement system to the animals' postmetamorphic existence. Although the adult fish has a bilaterally asymmetric appearance, the central nervous connectivity reestablishes symmetry in the vestibulo-oculomotor system.