Electrophysiological and Behavioral Evidence Demonstrating That Predator Detection Alters Adaptive Behaviors in the SnailLymnaea

Abstract

Stress has been shown to both impair and enhance learning, long-term memory (LTM) formation, and/or its recall. The pond snail, Lymnaea stagnalis, both detects and responds to the scent of a crayfish predator with multiple stress-related behavioral responses. Using both behavioral and electrophysiological evidence, this investigation is a first attempt to characterize how an environmentally relevant stressor (scent of a predator) enhances LTM formation in Lymnaea. Using a training procedure that, in "standard" pond water (PW), results in an intermediate-term memory that persists for only 3 h, we found that training snails in "crayfish effluent" (CE) induces a memory that persists for 48 h (i.e., its now an LTM). In addition, if we use a training procedure that in PW produces an LTM that persists for 1 d, we find that snails trained in CE have an LTM that persists for at least 8 d. Furthermore, we describe how a single neuron (RPeD1), which has been shown to be a necessary site for LTM formation, reflects the behavioral changes in its firing properties that persist for the duration of the LTM. Finally, Lymnaea exhibit context-specific memory, that is, when a memory is formed in a specific context (food odorant), it is only recalled in that context. Here, we found that snails trained in CE demonstrate context generalization, that is, memory is recalled in multiple contexts. All data are consistent with the hypothesis that learning in a stressful, yet biologically relevant, environment enhances LTM and prolongs its retention.

A flavonol, epicatechin, reverses the suppressive effects of a stressor on LTM formation

“…We arrived at that hypothesis based on earlier experiments with the simultaneous presentation of two different stressors that significantly alter LTM formation in Lymnaea. The two stressors used were: (1) low calcium, which as we have seen, suppresses LTM and (2) predator detection, which enhances LTM formation Dalesman et al, 2011c;Knezevic et al, 2011;Orr and Lukowiak, 2008). We found that operantly trained animals (two 0.5 h training sessions) that were held in the lowcalcium environment in the presence of CE, were able to form LTM lasting 24 h suggesting that training in CE may prevent the memory-blocking effects of a lowcalcium environment.…”

“…We have attempted to surmount these difficulties by using a simple model system (aerial respiratory behaviour in Lymnaea) in animals with a less-complex brain and a relatively simple tractable behaviour (Lukowiak et al, 1996;Lukowiak et al, 1998;Lukowiak et al, 2000). We have shown that different stressors significantly alter LTM formation and at the same time alters the excitability of a neuron (RPeD1) known to be a necessary locus of LTM formation (Scheibenstock et al, 2002;Sangha et al, 2003a;Sangha et al, 2003b;Sangha et al, 2003c;Sangha et al, 2005;Orr and Lukowiak, 2008;. Therefore, the changes effected in RPeD1 by the various stressors used are consistent with the observed effect of the stressor on LTM formation.…”

“…We have found that a wide variety of ecologically relevant stressors alter LTM formation Lukowiak et al, 2010). For example, detection of predator smells such as crayfish effluent (CE) enhanced both vigilance behaviours and LTM formation (Orr et al, 2007;Orr et al, 2009;Orr and Lukowiak, 2008); while crowding, low environmental calcium, and certain heavy metals (Zn and Cd) and H 2 S in pond water block LTM formation (Rosenegger et al, 2004;De Caigny and Lukowiak, 2008;Byzitter et al, 2012). A comprehensive summary of which ecologically relevant stressors significantly alter LTM formation can be found in two recent reviews (Lukowiak et al, 2014).…”

Heat stress enhances LTM formation inLymnaea: role of HSPs and DNA methylation

“…In the first procedure, snails received a single 0.5 h training session (TS1; Sangha et al, 2003;Parvez et al, 2005;Orr and Lukowiak, 2008;Teskey et al, 2012) and then a memory test session (MT) was performed 24 h after the TS1. In the second procedure, snails received two 0.5 h training sessions separated by a 1 h interval (i.e.…”

Discrimination learning with light stimuli in restrained American lobster

“…Electrophysiological techniques have been applied to the study of learning mechanisms in some invertebrates [39][40][41][42][43][44][45][46][47]. However, neurophysiological mechanisms responsible for their brain functions remain to be clarified at the level of identifiable nerve cells in the future chiefly because of experimental difficulties in recording their activities from freely behaving animals.…”