Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey

Abstract The reticulospinal system is the major descending pathway from the brain to the spinal cord in the sea lamprey, Petromyzon marinus . In order to determine the synaptic connections of this system and to gain a better understanding of its functions, individual cell bodies and axons of identified reticulospinal neurons were stimulated intracellularly while recording from spinal interneurons and motoneurons. Stimulation of reticulospinal axons of the bulbar and vagal groups produced unitary composite EPSP's in lateral cells. Both components of these EPSP's followed repetitive presynaptic action potentials one‐to‐one at constant short latencies. The first component was due to electrical coupling between the cell and axon. The second component was due to chemical transmission because it was eliminated after extracellular Ca was replaced with Mg and because it changed in amplitude during repeated stimulation. Evidence is presented that the second component, as well as the first, is monosynaptic. Both fast and slow motoneurons to myotomal muscle received a predominantly electrical synapse from the Müller axon I 1 . They also exhibited composite EPSP's after stimulation of M1, M3, some bulbar cells, and the Mauthner cell. Stimulation of ventral roots produced depolarizations in Müller axons which excited motoneurons. Polysynaptic EPSP's were observed in a fin motoneuron after stimulation of the contralateral axon M3 or I 1 . Some edge cells exhibited a composite EPSP after stimulation of the bursting axon I 2 . Morphologically mixed synapses with both chemical and electrical junctions were observed between Müller axons and unidentified dendrites. The cells of origin of the bursting axons were the pair I 2 . Stimulation of these axons in situ produced either no movements or weak fin movements. No synaptic potentials were observed in motoneurons in the cord or in bulbar cells in the brain after stimulation of I 2 . Intracellular stimulation of giant interneurons produced EPSP's in one pair of bulbar cells. The conclusions drawn from this and the preceding study are as follows: (a) Connections of identified neurons in the lamprey are specific but do not always occur. (b) The majority of synapses from large axons to identified cells utilize dual electrical and chemical transmission. (c) Most unitary EPSP's are subthreshold. Thus, other sources of excitation, especially from smaller unidentified neurons, are required for activity.