Electrophysiological characteristics of feeding-related neurons after taste avoidance Pavlovian conditioning in Lymnaea stagnalis

Abstract

Taste avoidance conditioning (TAC) was carried out on the pond snail, Lymnaea stagnalis. The conditional stimulus (CS) was sucrose which elicits feeding behavior; while the unconditional stimulus (US) was a tactile stimulus to the head which causes feeding to be suppressed. The neuronal circuit that drives feeding behavior in Lymnaea is well worked out. We therefore compared the physiological characteristics on 3 classes of neurons involved with feeding behavior especially in response to the CS in conditioned vs. control snails. The cerebral giant cell (CGC) modulates feeding behavior, N1 medial neuron (N1M) is one of the central pattern generator neurons that organizes feeding behavior, while B3 is a motor neuron active during the rasp phase of feeding. We found the resting membrane potential in CGC was hyperpolarized significantly in conditioned snails but impulse activity remained the same between conditioned vs. control snails. There was, however, a significant increase in spontaneous activity and a significant depolarization of N1M’s resting membrane potential in conditioned snails. These changes in N1M activity as a result of training are thought to be due to withdrawal interneuron RPeD11 altering the activity of the CGCs. Finally, in B3 there was: 1) a significant decrease in the amplitude and the frequency of the post-synaptic potentials; 2) a significant hyperpolarization of resting membrane potential in conditioned snails; and 3) a disappearance of bursting activity typically initiated by the CS. These neuronal modifications are consistent with the behavioral phenotype elicited by the CS following conditioning.

Lymnaea stagnalis as model for translational neuroscience research: From pond to bench

“…The ability of snails to undergo configurational learning is an ulterior confirmation of its potentiality in neuroscience and behavioural research (Swinton et al, 2019). Depending on the training procedure used, either intermediate term-memory (ITM; persisting up to 3 h) or LTM (persisting for at least 24 h) occurred in L. stagnalis (Kojima et al, 1996;Benjamin et al, 2000;Sangha et al, 2003c;Ito et al, 2013;Otsuka et al, 2013;Takahashi et al, 2013;Lukowiak et al, 2014;Sunada et al, 2014). Because the inhibition of transcription or translation blocked the formation of LTM in a variety of model systems, but did not affect short-term memory (STM), it has been concluded that this phase, lasting only minutes, does not require neither de novo protein nor RNA synthesis (De Zazzo and Tully, 1995).…”

Memory block: A consequence of conflict resolution

“…Snails are able to consolidate the associative learning into long-term memory (LTM) (Benjamin et al, 2000;Otsuka et al, 2013;Takahashi et al, 2013;Lukowiak et al, 2014;Sunada et al, 2014). Here, we look at the ability of Lymnaea to learn and remember for many days not to respond to a food substance that normally elicits a feeding response.…”

Function of insulin in snail brain in associative learning

“…Because the B3 cell receives an inhibitory input from the N1M cell (Staras et al 1998;Fig. 2b), the B3 cell was expected to be suppressed in taste aversion-trained snails, and that is what they found (Sunada et al 2014).…”

“…From their experiments, they have constructed a model that differs from the Kojima model described above (Sunada et al 2014). In their model, there is no change in the synaptic input from the CGC to the N1M cell after CTA-LTM.…”