Organization of synaptic inputs to paracerebral feeding command interneurons of Pleurobranchaea californica. III. Modifications induced by experience

Abstract

Phasic paracerebral feeding command interneurons (PCP's) were studied in whole-animal preparations of Pleurobranchaea drawn from four populations with different behavioral histories: food avoidance conditioned, yoked controls, food satiated, and naive. PCP responses to chemosensory food stimuli (liquefied squid) and mechanosensory touch stimuli (tactile stimulation of anterior and posterior structures) were recorded intracellularly, scored blind, and compared quantitatively across the four populations. PCP's from avoidance-conditioned specimens (10, 18, 19) showed decreased excitatory and increased inhibitory responses to food and touch in comparison with naive (untrained) specimens. Control animals did not show these effects. PCP's from satiated specimens showed decreased excitatory and increased inhibitory responses to food and touch in comparison with PCP's from control, naive, and conditioned specimens. Inhibitory postsynaptic potentials (IPSPs) induced in PCP's of conditioned and satiated specimens by food and touch are indistinguishable in amplitude and waveform from IPSPs produced in the same PCP's by the previously described cyclic inhibitory network (CIN; Ref. 13). In addition, tonic paracerebral neurons (PCT's) that lack input from the CIN, are not inhibited but rather are excited in trained and satiated animals. Therefore the inhibitory responses to food and touch by PCP's of conditioned and satiated specimens appear to be mediated by the CIN. This study demonstrates that associative and nonassociative processes (learning and food satiation, respectively) manifest similarly at the level of command interneurons. The findings furnish a neurophysiological explanation for behavioral motivation in Pleurobranchaea, namely, modulation of the balance of excitation/inhibition in command neurons controlling the corresponding behavior. A cellular model of food avoidance learning and food satiation is formulated to account for these data, based on the identified neural circuitry of the paracerebral command system (15, 17).