Central mechanisms underlying fish swimming

Abstract

Although the basic swimming rhythm is created by central pattern generators (CPGs) located in each spinal segment, command signals from the brain should be indispensable for the activation of CPGs to initiate swimming. We hypothesized that the nucleus of medial longitudinal fascicles (Nflm) is the midbrain locomotor region driving swimming rhythms in teleosts. To test this hypothesis, we recorded neuronal activities from Nflm neurons in swimming carp and analyzed the cytoarchitecture of the nucleus. We identified two types of Nflm neurons exhibiting electric activities closely related to swimming rhythms. Remarkably, tonic neurons that continued firing during swimming were found. The Nflm and neighboring oculomotor nucleus contain about 600 neurons in total, and among them as many as 500 were labeled retrogradely by an intraspinal tracer implantation and 400 neurons showed glutamatergic immunoreactivity. They are the most likely candidates for the descending neurons as the origin of driving signals that initiate swimming. Double-labeling experiments demonstrated direct connections of Nflm neurons to spinal neurons consisting of the CPG. These data imply that most Nflm neurons possibly exert an excitatory drive to the spinal CPGs through the descending axons with excitatory transmitter(s), probably glutamate. Furthermore, we confirmed that the caudal part of Nflm and the rostral part of the oculomotor nucleus overlap rostrocaudally by approximately 200 mum. In connection with the control of swimming by the brain, we carried out experiments to clarify the efferent system of the cerebellum of the goldfish. Cerebellar efferent fibers terminated in most brain regions except for the telencephalon. Importantly, the cerebellum projected also to the Nflm, suggesting the involvement of this brain region in the control of swimming. We have also determined that in the carp so-called eurydendroid cells are cerebellar efferent neurons.