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

Abstract

One of the most widely accepted benefits of enhanced physical activity is an improvement in the symptoms of depression, including the facilitation of decision making. Up until now, these effects have been shown in rodents and humans only. Little is known about their evolutionary origin or biological basis, and the underlying cellular mechanisms also remain relatively elusive. Here, we demonstrate for the first time that preceding motor activity accelerates decision making in an invertebrate, the pond snail Lymnaea stagnalis. To investigate decision making in a novel environment, snails, which normally live in water, were placed on a flat dry surface to simulate the potentially threatening consequence of being in an arid environment. This stimulus initiated two distinct phases in snail behaviour: slow circular movements, followed by intense locomotion in a chosen direction. The first phase was prolonged when the test arena was symmetrically lit, compared with one with an apparent gradient of light. However, forced muscular locomotion for 2 h prior to the test promoted the transition from random circular motions to a directional crawl, accompanied by an increase in crawling speed but with no effect on the choice of direction. Intense locomotion for 2 h also produced a strong excitatory effect on the activity of serotonergic neurons in L. stagnalis. Our results suggest that the beneficial effects of physical exercise on cognitive performance in mammals might have deep roots in evolution, granting the opportunity to unravel the origins of such effects at the single-neuron and network levels.

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

“…Previously, we reported that the behavioral effects of intense locomotion in the Lymnaea stagnalis snail are, in many aspects, similar to those observed in rodents and humans, with a decrease in defensive responses, an increase in general activity (D'yakonova, 2014) and a facilitation of decision-making in the novel environment (Korshunova et al, 2016). Terrestriallike crawling in low water for 2 h prior to the test promoted the transition from slow circular locomotion to the fast goaloriented crawl in asymmetrically lit arena (Korshunova et al, 2016). We concluded that exercise "facilitates the transition from uncertainty to decision-making in snails.…”

“…Enhanced motor activity was evoked (as in Korshunova et al, 2016) by putting the snails into a tank (50 × 50 cm) filled with 1-2 mm layer of water for 2 or 4 h. As was reported earlier this procedure "protected snails from drying but forced them to use intense muscular crawling to compensate for the lack of water supporting the weight of their shells" (Korshunova et al, 2016, Figure 1A). Control snails were kept in deep water so they could use ciliary locomotion in similar light conditions.…”

“…The influence of physical exercise on brain function has been thoroughly investigated in various mammalian species (van Praag et al, 1999;Salmon, 2001;Cotman et al, 2007;Hillman et al, 2008;Roig et al, 2012;Laurence et al, 2015). It has been suggested that feedforward brain activation caused by intense locomotion is a widespread phenomenon throughout the animal kingdom that may be especially beneficial for subsequent orientation and adaptation in the novel environment (Stevenson et al, 2005;Dyakonova and Krushinsky, 2008;Korshunova et al, 2016).…”

“…Activation of BDNF synthesis and release, known to have strong interactions with the serotonergic system (Popova et al, 2017), is required to mimic these effects (Choi et al, 2018). Strong effects of intense locomotion on subsequent behavior are reported in a distantly related group of animals, the protostomes (Hofmann and Stevenson, 2000;Dyakonova and Krushinsky, 2008;Korshunova et al, 2016), suggesting that mechanisms other than augmentation of hippocampal neurogenesis can mediate the behavioral benefits of exercise.…”

Olfactory navigation in aquatic gastropods

“…Other gastropods, such as T. diomedea and H. crassicornis, use cilia to crawl, and ciliary motor neurons have been identified in both species (Audesirk, 1978;Cain et al, 2006;Crow and Tian, 2003;Popescu and Willows, 1999;Willows et al, 1997). In L. stagnalis, crawling can be ciliary or muscular, resulting in two different speeds of locomotion (Korshunova et al, 2016;Pavlova, 2010), although the two systems may have a common serotonergic innervation (but see Longley and Peterman, 2013). Motor neurons controlling turns have also been studied in some gastropods.…”