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.

To elucidate mechanisms that underlie the profound physiological effects of the monoamine precursors 5-hydroxy-L-tryptophan (5-HTP) and L-3,4-dihydroxyphenylalanine (L-DOPA), we examined their action on single monoaminergic neurons isolated from the ganglia of the gastropod snail Lymnaea stagnalis. In isolated serotonergic PeA motoneurons, 5-HTP produced excitation. The effect was mimicked by serotonin at 0.5-1 microM, masked by pretreatment with serotonin at higher concentrations, and abolished by the inhibitor of aromatic amino acid decarboxylase (AAAD) m-hydroxybenzylhydrazine (NSD-1015), the inhibitor of the vesicular monoamine transporter reserpine or the serotonin receptor antagonist mianserin. Exposure of the dopaminergic interneurons RPeD1 to L-DOPA caused a biphasic effect composed of a depolarization followed by a hyperpolarization. AAAD inactivation with NSD-1015, as well as the blockade of dopamine receptors with sulpiride, resulted in the enhancement of the excitatory effect, and the abolition of the inhibitory effect. Dopamine caused hyperpolarization and masked the inhibitory phase of L-DOPA action. The results show that precursors affect the rate of firing of isolated monoaminergic neurons and that their effect is completely or partially mediated by the enhanced synthesis of the respective neurotransmitter, followed by extrasynaptic release of the latter and activation of extrasynaptic autoreceptors.

Benefits of physical exercise for brain functions are well documented in mammals, including humans. In this review, we will summarize recent research on the effects of species-specific intense locomotion on behavior and brain functions of different invertebrates. Special emphasis is made on understanding the biological significance of these effects as well as underlying cellular and molecular mechanisms. The results obtained in three distantly related clades of protostomes, Nematodes, Molluscs and Artropods, suggest that influence of intense locomotion on the brain could have deep roots in evolution and wide adaptive significance. In C. elegans, improved learning, nerve regeneration, resistance to neurodegenerative processes were detected after physical activity; in L. stagnalis—facilitation of decision making in the novel environment, in Drosophila—increased endurance, improved sleep and feeding behavior, in G. bimaculatus—improved orientation in conspecific phonotaxis, enhanced aggressiveness, higher mating success, resistance to some disturbing stimuli. Many of these effects have previously been described in mammals as beneficial results of running, suggesting certain similarity between distantly-related species. Our hypothesis posits that the above modulation of cognitive functions results from changes in the organism’s predictive model. Intense movement is interpreted by the organism as predictive of change, in anticipation of which adjustments need to be made. Identifying the physiological and molecular mechanisms behind these adjustments is easier in experiments in invertebrates and may lead to the discovery of novel neurobiological mechanisms for regulation and correction of cognitive and emotional status.

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It is well known that most rhythm-generating neuronal ensembles are multifunctional and can generate different motor rhythms in different contexts. This implies that coordination of multifunctional networks must also be flexible or multistable. Coordination of radula movements and gut contractions was studied in semi-intact preparations of L. stagnalis using video registration and an event recorder. Several context-dependent stable variants of radula-gut coordination were detected. Our data suggest that this preparation is a promising model for studying mechanisms of multistable motor rhythm coordination.