Synaptic potentials in common snail muscles during stimulation of command neurons.

Abstract

Giant defensive behavior command neurons have extensive efferent outputs to the muscles of the body wall and mantle of the common snail. Neurons in the mediorostral zone of the parietal ganglia, i.e., neurons LPa2, LPa3, RPa2, and RPa3, send processes via most of the visceral nerves, the pedal nerves, and the cutaneous nerves of the pedal ganglia [1, 3]. Command neurons trigger contraction of the pneumostoma and a series of somatic muscles. In addition, these cells send synaptic potentials to the heart and the walls of the pulmonary cavity [2, 4]. We have observed that activation of command neurons in the parietal ganglia leads to the appearance of postsynaptic potentials (PSP) in many visceral muscles and in the walls of some internal organs. These data were obtained using a new modification of the semi-intact preparation in which virtually all neuroeffector connections are preserved [5]. Command neuron activity was recorded by standard microelectrode techniques. Postsynaptic potentials were recorded using macroelectrodes consisting of glass pipettes with tip diameters of 100‐250 μm. Macroelectrodes were attached to flexible polyethylene tubing and filled with physiological saline. Large muscles were studied by inserting the electrode into the muscle, while thin-walled organs were studied by recording potentials from the surface. Activation of command neurons LPa2 and RPa2, as well as RPa3, induced postsynaptic potentials in the heart, pericardium, the wall of the pulmonary cavity, the columellar muscle, the muscles of the mantle ridge and body wall, the walls of the kidney, the antenna tip retractors, and the cerebral artery. In all cases, postsynaptic potentials showed marked facilitation during rhythmic neuron discharges. The first postsynaptic potential following a prolonged period of rest was sometimes below the noise level. In these cases, the coefficient of facilitation was taken as the ratio to the second postsynaptic potential. The coefficient of facilitation during prolonged series of neuron discharges could reach values of the order of 20 or more (Fig. 1. A). Series of postsynaptic potentials in command neurons were accompanied by long-lasting potentiating effects, which then decreased with a time constant of 3‐4 min. Facilitation and potentiation of postsynaptic potentials occurred differently in different neurons. This is evidence for the absence of any common terminal switching. The latent periods of postsynaptic potentials varied slightly from preparation to preparation and depend on the recording site. The latent periods of postsynaptic potentials at different points can be compared from the results presented from one animal (Fig. 2). In this experiment, postsynaptic potentials were sequentially recorded from eight different points in conditions of stimulation of LPa2 and RPa2, as well as RPa3. After action potentials in neuron RPa3, the shortest-latency postsynaptic potentials arose in the spurs of the columellar muscle and the wall of the cerebral artery (about 110 msec), while the longest delays were recorded in the mantle (160 msec; Fig. 2, B). Comparison of postsynaptic potentials from different neurons but at the same point showed that postsynaptic potentials from neuron RPa2 appeared in the mantle muscles 25‐30 msec earlier than those from RPa3 (Fig. 2, C). Analysis of the latent periods of postsynaptic potentials at different points showed that in general, changes in potentials from one recording point to another corresponded to the probable changes in the length of the pathways for the neuronal action potentials. Over the range recorded, delays corresponded quite closely to data obtained by Wilgenburg and Milligan [4], who measured the latent periods between action potentials in cell B (terminology used at that time;