The Activity of Isolated Neurons and the Modulatory State of an Isolated Nervous System Represent a Recent Behavioural State

Abstract

Behavioural/motivational state is known to influence nearly all aspects of physiology and behaviour. The cellular basis of behavioural state control is only partially understood. Our investigation, performed on the pond snail Lymnaea stagnalis whose nervous system is useful for work on completely isolated neurons, provided several results related to this problem. First, we demonstrated that the behavioural state can produce long-term changes in individual neurons that persist even after neuron isolation from the nervous system. Specifically, we found that pedal serotonergic neurons that control locomotion show higher activity and lower membrane potential after being isolated from the nervous systems of hungry animals. Second, we showed that the modulatory state (the chemical neuroactive microenvironment of the central ganglia) changes in accordance with the nutritional state of an animal and produces predicted changes in single isolated locomotor neurons. Third, we report that observed hunger-induced effects can be explained by the increased synthesis of serotonin in pedal serotonergic neurons, which has an impact on the electrical activity of isolated serotonergic neurons and the intensity of extrasynaptic serotonin release from the pedal ganglia.

Previous motor activity affects transition from uncertainty to decision-making in snails

“…Lymnaea stagnalis has been used widely for analysis of the cellular and molecular mechanisms of behaviour (Dyakonova et al, 2015;Koene, 2010;Marra et al, 2013;Pirger et al, 2014;Schmold and Syed, 2012), including studies at the single-cell level (Dyakonova et al, 2009(Dyakonova et al, , 2015Dyakonova and Dyakonova, 2010;Schmold and Syed, 2012). Therefore, our findings also reveal new opportunities for investigating the cellular basis of the intriguing interplay between motor and cognitive activities, which may have deep roots in evolution.…”

“…Lymnaea stagnalis snails have been used extensively for the analysis of cellular and molecular mechanisms of locomotion (Syed and Winlow, 1991b;Pavlova, 2010;Longley and Peterman, 2013), feeding (Benjamin and Rose, 1979;Elliott and Benjamin, 1989;Kemenes and Elliott, 1994;Staras et al, 1998Staras et al, , 2003Alania et al, 2004;Vehovszky et al, 2005;Vavoulis et al, 2007;Chistopolsky and Dyakonova, 2012), respiration (Syed and Winlow, 1991a,b;Tsyganov et al, 2004;Bell et al, 2007), learning and memory (Kemenes et al, 1997(Kemenes et al, , 2002Kojima et al, 1997;Spencer et al, 1999;Staras et al, 1998;Jones et al, 2003;Sangha et al, 2003;Kemenes et al, 2006;Nikitin et al, 2008;Marra et al, 2013;Mita et al, 2014;Naskar et al, 2014), and decision making (Pirger et al, 2014;Crossley et al, 2016). There are also approaches that have been developed only in this organism, particularly the studies at the single-cell level of freshly isolated, not cultured, neurons (Dyakonova et al, 2009(Dyakonova et al, , 2015Dyakonova and Dyakonova, 2010), and experimental tests of an extracellular chemical microenvironment that has been demonstrated to play a prominent 'socializing' role in adjusting single-cell physiology to the network state (Dyakonova et al, 2015). The neurons that control locomotion are at least partially known (Longley and Peterman, 2013).…”

“…Among them are serotonergic PeA cells forming a big cluster in the pedal ganglia (Syed and Winlow, 1989). As the extra-synaptic release of a neurotransmitter was demonstrated for these neurons, they have been suggested to have a prominent neuromodulatory role (Chistopol'skii and Sakharov, 2003;Dyakonova et al, 2015). Our preliminary results show that 2 h of intense locomotion produce a strong excitatory effect on the activity of PeA cells (68±5 versus 13.5±3 action potential min −1 in control, N=14, Mann-Whitney U-test, z=2.96; P<0.003).…”

The Role of Serotonin in the Influence of Intense Locomotion on the Behavior Under Uncertainty in the Mollusk Lymnaea stagnalis

“…The neurons that control locomotion in L. stagnalis include a large serotonergic PeA cluster of cells which release serotonin to the muscles and cilia in the sole (Syed and Winlow, 1989;Longley and Peterman, 2013). The PeA neurons have also been suggested to have a neuromodulatory and neurohormonal role in the central nervous system (Chistopol'skii and Sakharov, 2003;Dyakonova et al, 2015). Many of the above-mentioned behavioral effects of exercise are similar to the influences ascribed to the increased level of serotonin in Lymnaea.…”

A central control circuit for encoding perceived food value

“…This animal generates clearly definable ingestion and egestion behaviors using a wellidentified CPG (Straub et al, 2002;Vavoulis et al, 2007) that drives a highly complex feeding musculature consisting of 46 muscles (Benjamin, 2012). This system offers a unique entry point for elucidating fundamental mechanisms that encode changes in motivational state and direct the expression of relevant animal behavior (Crossley et al, 2016;Dyakonova et al, 2015;Staras et al, 2003).…”