Using an invertebrate model to investigate the mechanisms of short-term memory deficits induced by food deprivation

Abstract

Although prolonged food deprivation is known to cause memory deficits, the underlying mechanisms are only partially understood. In this study, we began to investigate the cellular substrates of food deprivation-induced memory impairments in the invertebrate Aplysia. Following a single trial of noxious stimuli, Aplysia concurrently express short-term sensitization (an elementary form of learning in which withdrawal reflexes are enhanced) and short-term feeding suppression for at least 15 min. Cellular correlates of sensitization and feeding suppression include increased excitability of the tail sensory neurons (TSNs) controlling the withdrawal reflexes, and decreased excitability of feeding decision-making neuron B51, respectively. Recently, 14 days of food deprivation (14DFD) was reported to break the co-expression of sensitization and feeding suppression in Aplysia without health deterioration. Specifically, under 14DFD, sensitization was completely prevented while feeding suppression was present albeit attenuated. This study explored the cellular mechanisms underlying the absent sensitization and reduced feeding suppression under 14DFD. A reduced preparation was used to evaluate the short-term cellular modifications induced by delivering an aversive training protocol in vitro. TSN excitability failed to increase following in vitro training under 14DFD, suggesting that the lack of sensitization may be a consequence of the fact that TSN excitability failed to increase. B51 excitability also failed to decrease following in vitro training, indicating that additional neurons may contribute to the conserved albeit reduced feeding suppression in 14DFD animals. This study lays the foundations for the future use of the Aplysia model system to investigate the mechanisms underlying the memory impairments induced by prolonged food deprivation.

Keywords: Excitability; Feeding suppression; Food deprivation; Memory; Short-term sensitization.

Figure. 1.

Feeding regimens, configuration of the in vitro preparation, and experimental protocols. (A) Animals were randomly assigned to 2DFD or 14DFD regimens. (B) The in vitro preparation consisted of buccal, cerebral and pleural-pedal ganglia. One of the two buccal nerves n.2,3 (arrow) was retained for electrophysiological identification of B51. Pedal nerves P8 and P9 were retained for the simultaneous delivery of electrical shocks. (C) Protocol describing the recordings of TSNs and B51 and the single-trial in vitro training (lightning bolt). Membrane properties measured in TSNs included resting potential and number of spikes. Membrane properties recorded in B51 included resting potential, input resistance, and burst threshold. Properties of TSNs and B51 were measured 10 min prior to training. Post-tests of TSNs were conducted 5 min and 15 min after training. Post-test of B51 was conducted 15 min after training.

Figure 2.

14DFD prevented increased excitability of TSNs both 5 min and 15 min after in vitro training. (A) Sample traces of TSNs spikes in pre-tests, 5-min and 15-min post-tests in each of the four groups used. Summary data illustrate that increased excitability of TSNs was absent in 14D-T preparations but was observed in 2D-T preparations 5 min (B1) and 15 min (B2) after training.

Figure 3.

14DFD prevented decreased excitability of B51 15 min after in vitro training. (A) Sample traces of B51 burst threshold in pre-tests and 15-min post-tests in the four groups used. (B) Summary data reveal that 15 min after training, B51 decreased excitability was absent in 14D-T preparations, but it was observed in 2D-T preparations.