Phasic Coordination between Locomotor and Respiratory Rhythms in the Mollusk Lymnaea: Transmitter-Specific Modifications

Tsyganov, Vladimir; Vorontsov, Dmitry D.; Sakharov, D. A.

doi:10.1023/b:dobs.0000025229.83826.d9

Cited by 5 publications

(5 citation statements)

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“…In looking for possible neurotransmitters that might explain the masking effect in the CNS of ER snails we considered the dopaminergic system. Opposite effects of serotonin and dopamine on locomotor behavior have been found in several mollusk species 25–27 . To test possible involvement of dopamine, the dopamine antagonist sulpiride (0.01–0.1 mM) was added to the dish containing CNS preparations isolated from the control and ER snails.…”

Section: Resultsmentioning

confidence: 99%

Storage and erasure of behavioural experiences at the single neuron level

D'yakonova

Sultanakhmetov

Mezheritskiy

et al. 2019

Sci Rep

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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.

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Section: Resultsmentioning

confidence: 99%

Storage and erasure of behavioural experiences at the single neuron level

D'yakonova

Sultanakhmetov

Mezheritskiy

et al. 2019

Sci Rep

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“…This suggestion is in line with the effects of serotonergic drugs in mollusks reported earlier. Activation of the aquatic and terrestrial locomotion in Lymnaea stagnalis by serotonin or 5-HTP was found in several studies (Pavlova, 2001(Pavlova, , 2019Tsyganov et al, 2004). Activation of searching movements by serotonin was shown in the terrestrial snails Helix (Roshchin and Balaban, 2012) and Cepaea (Dyakonova et al, 1995).…”

Section: Serotonin and Behavioral Changes Caused By Preceding Intensementioning

confidence: 87%

“…The Effect of Serotonin Metabolic Precursor 5-Hydroxytryptamine (5-HTP) on Snail Behavior on the Dry Surface (Experiment 3) 5-HTP is known to increase the speed of locomotion in Lymnaea (Pavlova, 2001(Pavlova, , 2019Tsyganov et al, 2004). Here we found that the snails immersed in 5-HTP (n = 27) demonstrated a more rapid onset of activity compared to the control group (n = 27).…”

Section: The Effects Of Pharmacological Manipulations With the Serotomentioning

confidence: 99%

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

et al. 2020

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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.

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“…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).…”

Section: Risky Decision Making By Snails In a Vital Situationmentioning

confidence: 99%

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

Korshunova

Vorontsov

Dyakonova

2016

Journal of Experimental Biology

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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.

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Phasic Coordination between Locomotor and Respiratory Rhythms in the Mollusk Lymnaea: Transmitter-Specific Modifications

Cited by 5 publications

References 2 publications

Storage and erasure of behavioural experiences at the single neuron level

Storage and erasure of behavioural experiences at the single neuron level

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

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

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