The role of serotonin in the immediate and delayed influence of physical exercise on brain functions has been intensively studied in mammals. Recently, immediate effects of intense locomotion on the decision-making under uncertainty were reported in the Great Pond snail, Lymnaea stagnalis (Korshunova et al., 2016). In this animal, serotonergic neurons control locomotion, and serotonin modulates many processes underlying behavior, including cognitive ones (memory and learning). Whether serotonin mediates the behavioral effects of intense locomotion in mollusks, as it does in vertebrates, remains unknown. Here, the delayed facilitating effects of intense locomotion on the decision-making in the novel environment are described in Lymnaea. Past exercise was found to alter the metabolism of serotonin, namely the content of serotonin precursor and its catabolites in the cerebral and pedal ganglia, as measured by highperformance liquid chromatography. The immediate and delayed effects of exercise on serotonin metabolism were different. Moreover, serotonin metabolism was regulated differently in different ganglia. Pharmacological manipulations of the serotonin content and receptor availability suggests that serotonin is likely to be responsible for the locomotor acceleration in the test of decision-making under uncertainty performed after exercise. However, the exercise-induced facilitation of decision-making (manifested in a reduced number of turns during the orienting behavior) cannot be attributed to the effects of serotonin.

Although predictions from the past about the future have been of major interest to current neuroscience, how past and present behavioral experience interacts at the level of a single neuron remains largely unknown. Using the pond snail Lymnaea stagnalis we found that recent experience of terrestrial locomotion (exercise) results in a long-term increase in the firing rate of serotonergic pedal (PeA) neurons. Isolation from the CNS preserved the “memory” about previous motor activity in the neurons even after the animals rested for two hours in deep water after the exercise. In contrast, in the CNS, no difference in the firing rate between the control and “exercise-rested” (ER) neurons was seen. ER snails, when placed again on a surface to exercise, nevertheless showed faster locomotor arousal. The difference in the firing rate between the control and ER isolated neurons disappeared when the neurons were placed in the microenvironment of their home ganglia. It is likely that an increased content of dopamine in the CNS masks an increased excitation of PeA neurons after rest: the dopamine receptor antagonist sulpiride produced sustained excitation in PeA neurons from ER snails but not in the control. Therefore, our data suggest the involvement of two mechanisms in the interplay of past and present experiences at the cellular level: intrinsic neuronal changes in the biophysical properties of the cell membrane and extrinsic modulatory environment of the ganglia.

In the cricket Gryllus bimaculatus, flying occurs soon after the last imaginal molt and precedes the mating behavior in natural conditions. Here, we tested the hypothesis that flying may improve subsequent behavioral performance in a novel environment in female crickets. We developed a behavioral set-up to test female cricket responsiveness to male calling song as well as their ability to locate and find the source of the song. The male song was produced by a loudspeaker hidden behind the fabric wall of a spacious square arena. Forced flight prior to the test promoted female sexual searching behavior in the novel environment. After the flight, more females reached the hidden source zone, spent more time near the source and finally more of them climbed over the wall section immediately in front of the hidden loudspeaker. At the same time, their behavior in the arena did not differ from the control group when the calling song was not delivered, suggesting that flight exerts its behavioral effects by influencing sexual motivation. Our results support the suggestion that preceding intense locomotion facilitates sexual searching behavior of females in a novel environment.

This review is devoted to the analysis of works that investigated the long-term effects of species-specific forms of intensive locomotion on the cognitive functions of animals and humans, which can be transmitted to the next generation. To date, the anxiolytic and cognitive-enhancing long-term effects of intensive locomotion have been demonstrated in humans, rodents, fish, insects, mollusks, and nematodes. In rodents, changes in the central nervous system caused by intense locomotion can be transmitted through the maternal and paternal line to the descendants of the first generation. These include reduced anxiety, improved spatial learning and memory, increased levels of brain neurotrophic factor and vascular endothelial growth factor in the hippocampus and frontal cortex. The shift of the balance of histone acetylation in the hippocampus of rodents towards hyperacetylation, and the balance of DNA methylation towards demethylation manifests itself both as a direct and as a first-generation inherited effect of motor activity. The question about the mechanisms that link locomotion with an increase in the plasticity of a genome in the brain of descendants remains poorly understood, and invertebrate model organisms can be an ideal object for its study. Currently, there is a lack of a theoretical model explaining why motor activity leads to long-term improvement of some cognitive functions that can be transmitted to the next generation and why such an influence could have appeared in evolution. The answer to these questions is not only of fundamental interest, but it is necessary for predicting therapeutic and possible side effects of motor activity in humans. In this regard, the article pays special attention to the review of ideas on the evolutionary aspects of the problem. We propose our own hypothesis, according to which the activating effect of intensive locomotion on the function of the nervous system could have been formed in evolution as a preadaptation to a possible entry into a new environment.

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.