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 µm. 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.

Fish swim by undulatory contractions of the axial trunk musculature. It has been presumed that a descending signal from the brainstem activates central pattern generators in the spinal cord to make the swimming rhythm. In the carp the electrical or chemical stimulation of a mesencephalic nucleus, the nucleus fasciculi longitudinalis medialis (Nflm), could initiate swimming. However, it has not been established what signals originate from the Nflm in order to make the fish swim. The activity of the Nflm neurons was therefore examined electrophysiologically during fictive swimming in paralyzed carp. Three types of neuronal activities closely related to the swimming rhythms were obtained. The first type was a continuous tonic firing throughout an episode of fictive swimming. Neurons involved in this tonic activity may project to the spinal cord and contribute to the activation of spinal neurons to initiate fish swimming. The second type was accompanied by continual phasic firings occurring in rhythm with the activity of spinal motoneurons. Supposing that the swimming rhythm originates in the spinal cord, the synchronous activity in the brain neurons may suggest that in the nucleus there is a relay neuron conveying the rhythm information from the cord to other neurons there or in the brain. The third type exhibited reduced firing rates during fictive swimming. It is possible that the neurons engaged in this activity may be inhibitory and suppress the activities of other neurons in the nucleus and spinal cord during rest or during decelerating swimming.

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