Abstract
Long-term changes in membrane potential after associative training were described previously in identified premotor interneurons for withdrawal of the terrestrial snail Helix. Serotonin was shown to be a major transmitter involved in triggering the long-term changes in mollusks. In the present study we compared the changes in electrophysiological characteristics of identifiable premotor interneurons for withdrawal in response to bath applications of serotonin (5-HT) or serotonin precursor 5-hydroxytryptophan (5-HTP) in preparations from naïve, neurotoxin-injected or associatively trained snails. It was found that 5-HT or 5-HTP applications caused a significant decrease of membrane potential in premotor interneurons of naïve snails, associatively trained snails and snails with impaired serotonergic system by injection of a selective neurotoxin 5,7-dihydroxytryptamine (5,7-DHT) 1 week before the experiments. Applications of 5-HT or 5-HTP did not cause significant changes in the action potential (AP) threshold potential of these neurons in naïve snails. Conversely, applications of 5-HT or 5-HTP to the premotor interneurons of previously trained or 5,7-DHT-injected snails caused a significant increase in the firing threshold potential in spite of a depolarizing shift of the resting membrane potential. Results demonstrate that responsiveness of premotor interneurons to extracellularly applied 5-HT or 5-HTP changes for days after the associative training or serotonin depletion. Similarity of the effects in trained and 5,7-DHT-injected animals may be due to massive release of serotonin elicited by 5,7-DHT injection. Our results suggest that serotonin release due to aversive conditionining or elicited by the neurotoxin administration triggers similar changes in resting membrane potential and AP threshold in response to bath applications of 5-HT or its precursor 5-HTP.
Highlights
Questions concerning the mechanisms of learning and memory are still open
Similar changes were observed after application of 5-HTP (Figure 2)
In a separate series of experiments, we have studied the responses of the premotor interneurons LPa3 and RPa3 to applications of 5-HT or 5-HTP in preparations from the snails in which the serotonergic neurons were selectively impaired by injection of a neurotoxic analog of serotonin, 5,7-dihydroxytryptamine (5,7-DHT, details in Balaban et al, 1987)
Summary
Questions concerning the mechanisms of learning and memory are still open. Experimental data show that the cellular processes associated with learning occur at least at two levels: long-term modifications of the synaptic transmission efficiency (presynaptic level) and changes in the endogenous properties of the whole neuron and its membrane potential (postsynaptic level; Balaban, 2002, 2017; Crow, 2004; Hawkins et al, 2006; Jin et al, 2009; Saar and Barkai, 2009; Gainutdinov et al, 2011; Hu et al, 2011; Vasil’yeva et al, 2015). Several specific tasks can be distinguished within the problem of cellular mechanisms of learning These tasks include an analysis of the excitability of both presynaptic and postsynaptic structures, i.e., membrane characteristics of neurons and synaptic transmission (Alkon, 1984; Byrne, 1987; Frysztak and Crow, 1997; Bao et al, 1998; Cleary et al, 1998; Gainutdinov et al, 1998; Daoudal and Debanne, 2003; Gainutdinova et al, 2003; Mozzachiodi et al, 2008; Crow and Tian, 2009; Debanne and Poo, 2010; Glanzman, 2010; Mozzachiodi and Byrne, 2010; Gainutdinov et al, 2011; Cavallo et al, 2014a,b; Pivovarov et al, 2014), and in particular the role of persistent sodium current in mechanisms of neuronal plasticity (Kiss, 2003; Nikitin et al, 2006; Kiss et al, 2009; Nagakura et al, 2010). (Ierusalimskii and Balaban, 2010; Sakharov, 2012) the concept concerning that the volume (extra-synaptic) transmission of 5-HT plays a major role in the mechanisms of memory in mollusks was discussed. In snails with impaired 5-HT neurons both aversive learning and reconsolidation were impaired, suggesting a necessity of 5-HT for behavioral plasticity (Balaban et al, 2016)
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