The role of serotonin in the enhancement of long-term memory resulting from predator detection in Lymnaea

Abstract

SUMMARYSerotonergic systems play important roles in modulating stress-induced arousal and vigilance behaviours. The pond snail, Lymnaea, shows multiple defensive vigilance behaviours in response to the stress associated with predator detection. Predator detection elicited by crayfish effluent (CE), increases the time to re-emerge from the shell and enhances the shadow withdrawal response. More importantly, in Lymnaea, CE enhances the ability to form long-term memory (LTM). We investigated the role of the serotonergic system in these anti-predator responses in Lymnaea. Using a serotonin-receptor antagonist, mianserin, we found that two defensive vigilance behaviours (e.g. increasing the time to re-emerge from their shell and shadow response) elicited by CE were not observed when the serotonergic system was disrupted. Also, methysergide, another serotonin antagonist, blocked the enhanced LTM formation after training in CE. Importantly, mianserin did not alter LTM formation in pond water (PW). These data suggest that a serotonergic system is activated only when Lymnaea detect a predator. When snails were trained in CE using a training procedure that in PW produces a 24-h LTM, a more persistent form of LTM (5days) occurred. This more persistent form of LTM was abolished after mianserin treatment. Increasing 5-HT levels in the snail by the injection of 5-HT was also associated with enhanced LTM formation. Lastly, we tested whether the osphradium is implicated in CE detection and subsequent enhanced formation of LTM. Cutting the osphradial nerve to the CNS resulted in the loss of the ability to form enhanced LTM in CE. Together, these findings support the hypothesis that the serotonergic system plays a key role in modulating the predator-induced stress responses in Lymnaea.

Investigating candidate neuromodulatory systems underlying parasitic manipulation: concepts, limitations and prospects

“…Serotonin is widely present in the animal kingdom, and modulates important behaviours from simple taxis to memory, learning, response to stress, sexual and agonistic behaviour, physiological process (including control of energy balance), circadian rhythms and neurogenesis (Weiger, 1997;Harzsch et al, 1999;Il-Han et al, 2010;Zhang et al, 2011). The role of this biogenic amine in parasite-induced changes in behaviour has been reported in some host-parasite models (Table1) but without elucidation of how the parasite interferes with the host's serotonergic system.…”

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

“…However, since the effects of epicatechin shown here occur within minutes of testing, we do not believe epicatechin works via this mechanism. Finally, we know that although CE, which also enhances LTM formation, works via a serotonergic pathway (Il-Han et al, 2010), blocking this pathway using mianserin (a serotonin receptor antagonist) does not effect the same LTM enhancement induced by epicatechin (Fruson et al, 2012).…”

“…It has also been shown that a flavonoid, epicatechin, found in dark chocolate, green tea and red wine (Kühnau, 1976;Matsuoka et al, 1995;Galliet al, 2002;Youdim et al, 2002) enhances LTM formation in Lymnaea (Fruson et al, 2012). However, the enhancement brought about by epicatechin occurs via a different mechanism than that brought about by predator detection (Il-Han et al, 2010;Fruson et al, 2012).…”

Input from a chemosensory organ, the osphradium, does not mediate aerial respiration in Lymnaea stagnalis

“…However, our recent results suggest that although the osphradium may play a role in oxygen detection (Wedemeyer & Schild 1995, Kamardin et al 2001, severing the osphradial nerve does not affect aerial respiration during hypoxia when assessed using the number of breathing attempts during training (Il-Han et al 2010, Dalesman et al 2011. We therefore wanted to confirm whether or not severing the osphradial nerve altered basic aerial respiration behaviour.…”