Sole Smooth Muscle States Determine Gliding Rate in the Freshwater Snail Lymnaea stagnalis.
In vertebrates and invertebrates, studying the function of smooth musculature and ciliated epithelia in visceral ducts and organs may injure the tissues, leading to a loss of data. The foot sole of crawling gastropods contains both smooth muscle and ciliated epithelium, making it a unique model for investigating the function of these tissues.
Two types of crawling are known for gastropods (Trueman, man, 1983). Creeping by peristaltic muscular waves was studied in the terrestrial gastropods Helix. Haliotis, and Pomatias (Lissmann, 1945). Ciliary locomotion, when muscular contractions are not seen in the foot, was described for pond snails such as Lymnaea stagnalis (Lister, 1694: Kaiser, 1960).
In our previous studies, however, we presented evidence that the horizontal muscular system underlying the ciliated epithelium in the foot sole of L. stagnalis (Plesch et al., 1975) may be involved in gliding (Bakeeva et al., 1992; Pavlova, 2006, 2010), and gliding rate up to 80% is determined by muscular activity (Pavlova, 2010). The horizontal muscular system of the sole in L. stagnalis is composed of single-unit phasic smooth muscle (Bakeeva et al., 1992), a muscle type that is able to generate rhythmic contractions. Additionally, the muscle cells in this horizontal muscular system contain giant mitochondria (Bakeeva et al., 1992) and are morphologically identical to the cells that generate locomotory muscular waves in Helix aspersa (Rogers, 1969). The muscle cells in the horizontal muscular system are a target for serotonin (5-HT) and cyanide (Pavlova, 2010), an inhibitor of mitochondrial respiration. 5-HT stimulates peristaltic locomotory waves in the foot of H. lucorum (Pavlova, 2001) and the slug Deroceras reticulatus (Pavlova, 2006). 5-HT significantly increases locomotor activity in L. stagnalis (Syed et al., 1988; Pavlova, 1997, 2006, 2010). Cyanide blocks muscular waves in the foot of D. reticulatus (Pavlova, 2006) and significantly decreases locomotor activity in L. stagnalis (Pavlova, 2006, 2010). Neither 5-11T nor cyanide change ciliary beat frequency in the foot sole of L. stagnalis (Pavlova, 2010).
The tonus of the longitudinal sole muscle cells in the horizontal muscular system in L. stagnalis is reflected in the length of the foot sole which can vary widely during gliding and is directly correlated with the gliding rate (Pavlova, 1990). This linear relationship between locomotion rate and sole length was also found in H. lucorum and H. pomatia (Pavlova, 1994).
Phasic smooth muscle has several active states: tonic contraction, tonic relaxation, and rhythmic contractions. Each state is influenced by a neurotransmitter (Carew et al., 1974; Muneoka and Twarog, 1983). For instance, as mentioned above, 5-HT stimulates locomotory muscular waves in both H. lucorum (Pavlova, 2001) and D. reticulatus (Pavlova, 2006). In H. lucorum, dopamine (DA) decreases snail speed via tonic sole contraction; and ergometrine, a synthetic blocker of one dopamine receptor type in molluscs (Juel, 1983; Shozushima, 1984; Sakharov and Kabotyansky, 1986; Sawada and Maeno, 1987), increases snail speed via tonic sole extension (Pavlova, 2001).
In L. stagnalis, 5-HT and DA also control gliding. Using high-performance liquid chromatography (HPLC), a radio-enzymatic assay (REA), and cytochemistry, 5-HT and DA have been shown to localize to the pedal ganglia and the foot (McCaman et al., 1979; Elekes et at., 1991; Hetherington et al., 1994; McKenzie et al., 1998). Both 5-HT (see above) and ergometrine (Pavlova, 2010) stimulate and significantly increase locomotor activity.
Nevertheless, how L. stagnalis controls gliding rate is still unclear. The aim of this study was to clarify how 5-HT, DA, and ergometrine modify the linear relationship between locomotion rate and sole length in L. stagnalis (i.e., how they regulate snail speed via sole muscle states) and to compare these data with the effects of these substances on locomotion rate and sole length in H. lucorum (Pavlova, 2001).
We report that, in L. stagnalis, 5-HT. DA, and ergometrine modify the linear relationship in the same way as seen in H. lucorum (Pavlova, 2001). Additionally, when taken in conjunction with corresponding changes in locomotory waves in H. lucorum (Pavlova, 2001), these modifications describe the fundamental mechanisms for controlling phasic smooth muscles. This provides the basis for future studies of phasic smooth muscles in different organs and ducts in vertebrates and invertebrates. These data also allow us to continue to explore other mechanisms of gliding in L. stag-nalis such as the effects of other neurotransmitters on the linear relationship and the effects of neurotransmitters on ciliary activity.
A brief summary of how 5-117 injection increases the gliding rate in L. stagnalis has been published (Pavlova, 1997).
Materials and Methods
Adult freshwater snails Lymnaea stagnalis (Linnaeus, 1758; Gastropoda, Pulmonata, Basommatophora) were obtained from ponds in Moscow suburbs during the summer, kept in laboratory aquaria at room temperature, and fed with lettuce. Experiments were conducted using whole snails. Small snails, weighing 0.3-0.4 g with a shell length of 16-20 mm, were exposed to one of the test substances. Each observation occurred under stable conditions and took about 2 h, which allowed for plenty of measurements of sole length and gliding rate to determine their linear relationship. Large snails, weighing 3.5-6.0 g with a shell length of 35-42 mm, were injected to collect additional data. For these snails, substance concentrations steadily decreased within 20-30 min (unstable conditions). This did not allow us to determine a linear relationship between snail speed and sole length under these circumstances; the same was true in the case of Helix lucorwn (Pavlova, 2001) and L. stagnvlis (Pavlova, 1997).
Calculating the linear relationship between sole length and snail speed To determine whether there was a linear relationship between sole length and snail speed, uniform gliding (with no rhythmic or sporadic movements) of each snail was observed individually in a small or large right-angled aquarium containing 50 ml or 2.5 1 of dechlorinated tap water, respectively. Each snail was photographed at fixed intervals from 10 to 25 s as it glided on the marked front wall of the aquarium with its entire sole visible (Pavlova, 1990). This procedure usually took 120 mm, and the contours of the soles were transferred from serial photographs to graph paper and collated with respect to reference marks on the wall (Fig. 1). This resulted in several consecutive projections of the sole on the same sheet of paper. The length of the sole was measured as the distance between the rostral and caudal midpoints, and the snail speed for the rostral midpoint was calculated. Each sheet with constant sole length was selected for analysis. Thus, dozens of different sole lengths and corresponding snail speeds were obtained for each snail. On the basis of these data, a linear relationship between sole length and locomotion rate was calculated by least-squares regression.
Effects of 5-HT, DA, and ergometrine on sole length and snail speed
Sole lengths and snail speeds were measured twice for each snail: once while it was spontaneous gliding under normal conditions and once during its treatment (exposure/injection) with the effective concentration of a test substance (see below). For small snails, each substance was dissolved in 100 [micro]l of tap water, added to the water in the small aquarium, and gently mixed to the desired final concentration. The sole length and snail speed measurements resumed 10 min after stirring and lasted 60-120 min.
Large snails were injected as previously described (Pavlova, 1997). Each snail was removed from the aquarium and injected in the dorsal side of the foot near the caudal column. This area is insensitive to tactile stimulus, and the injections were usually not followed by significant withdrawal of the body into the shell. We injected a freshly prepared substance dissolved in Lymnaea physiological saline (0.2 ml) of the following composition (in mmol [l.sup.-]): 44 NaC1, 3 KCI, 4 Ca[C1.sub.2], 2 Mg[C1.sub.2], and 10 Tris HC1, pH 7.6 (Kits and Bos, 1982). The snail was then returned to the aquarium. Observations continued until there was an obvious decrease in the effect of the injection. Control snails were injected with the same volumes of physiological saline. Tests were excluded from consideration if injection caused significant withdrawal of the snail into its shell accompanied with ejection of hemolymph.
Effective 5-HT, DA, and ergometrine concentrations
We found effective concentrations of each substance that caused obvious, stable, and repeatable changes in gliding rate, sole length. or both. These concentrations were usually in the range of or slightly higher than those used in similar experiments on L. stagnalis (Syed et at., 1988), Tritonia diomedea (Willows et al., 1997), Helix pomatia (Sakharov and Salanlci, 1982), and Clione limacina (Sakharov and Kabotyansky, 1986).
To find a 5-HT (5-hydroxytryptamine creatinine sulfate complex. Sigma) concentration that caused long continuous locomotion of small snails, seven groups of individuals (n = in each group) were placed in seven glass tanks filled with 50 ml of dechlorinated tap water. Six of the tanks contained ascending concentrations of 5-HT from [10.sup.-9] to [10.sup.-4] mol [1.sup.-1] and the seventh (control) contained water. The number of crawling snails in each group was counted every 20 min for 2 h and was expressed as a percentage with the total number of snails in each group as 100%. The same procedure was used to determine an effective ergometrine (maleate, Sigma) concentration.
To find a DA (3-hydroxytyramine hydrochloride, Sigma) concentration, the locomotion of small snails was observed in 50 ml of dechlorinated tap water during 60 min and then at increasing DA concentrations ([10.sup.-5] to [10.sup.-5] mol [1.sup.-1]). Each exposure (about 1 h duration) was followed by washing.
Effective injection concentrations for ergometrine and DA were identified at random. Ascorbic acid (Sigma) was also used in each test with DA as an antioxidant (Sakharov and Kabotyansky, 1986). Each dose was equal to either 2 [micro]g [g.sup.-1] of body weight or a concentration of 50 [micro]mol [1.sup.-1].
To compare the length of the sole before and during treatment, the total number of sole length measurements under normal conditions and separately in the presence of a substance and the maximum sole length (average of the three highest values independent of conditions) were taken as 100% for each snail. The number of scorings in each sole length category of 50%-70%, 71%-80%, 81%-90%, and 91%-100% of the maximum were then counted for spontaneous gliding and gliding in the presence of a substance.
To compare snail speed (gliding rate) before and during treatment, a maximum locomotion rate (independent of conditions) was taken as 100% for each snail. The mean locomotion rates were then calculated for each sole length category (see above) under normal conditions and during treatment with a substance. In each series of experiments, data were then averaged for all snails.
We used the Student's t-test if results were greater than zero for each sole length category and 12 if they were equal to zero in any sole length category. To perform the [x.sup.2]-test and to compare sole lengths recorded under the different conditions, the total number of sole length measurements was divided into four groups: normal conditions or in the presence of a substance and, for both cases, when the sole was equal to 50%-89% or 90%-100% of the maximum sole length. To compare snail speed recorded under the different conditions, the locomotion rates were also divided into four groups: recorded under normal conditions or in the presence of a substance and, for both cases, when speed was [greater than or equal to]50% or >50% of the maximum speed. The same statistical analyses were used for H. lucorum (Pavlova, 2001).
Exposure to [10.sup.-4]mol [l.sup.-1] 5-HT stimulates continuous gliding
All small snails (n = 18 in three experiments) exposed to [10.sup.-4] mol [1.sup.-1] 5-HT demonstrated long, continuous gliding (Fig. 2). Gliding was intermittent in the same number of snails exposed to [10.sup.-5] mol [1.sup.-1] 5-HT, other concentrations, and water. Exposure to [10.sup.-4] mol [1.sup.-1] 5-HT was used in the following experiments with small snails.
Exposure to 5-HT increases snail speed and has no effect on sole length
The effect of 5-HT on a snail sole length and locomotion rate is shown in Figure 3A. The length of the sole directly correlated with the snail speed under normal conditions. The snail increased its speed 10 min after exposure to 5-HT. The increased speeds directly correlated with sole length, which varied but remained within the range recorded under normal conditions.
Mean values of sole length in snails (n = 11) under normal conditions and in the presence of 5-HT were similar
(t-test, P > 0.8 for each sole length category, Fig. 3B). However, mean snail speeds were higher in the presence of 5-HT than under normal conditions (t-test, P < 0.005 for each sole length category, Fig. 3C).
Thus, 5-HT shifts the linear relationship between sole length and snail speed upward along the axis of snail speed.
DA contracts the sole and proportionally decreases snail speed
In the presence of 1.6*[10.sup.-3] mol[l.sup.1] DA, small snails (n = 4) that demonstrated stable spontaneous gliding under normal conditions contracted the sole and significantly slowed their speed, which sometimes became intermittent. The same result was observed in other snails (n = 8) when the effect of DA was studied in the presence of [10.sup.-4] mol [1.sup.-1] 5-HT to stimulate continuous gliding and to increase the number of measurements (Fig. 4A). Mean values obtained in both series for all snails (n = 12) showed that DA significantly decreased sole length ([x.sup.2]-test, P < 0.001, Fig. 4B) and snail speed ([x.sup.2]-test, P < 0.001, Fig. 4C).
DA slows the gliding rate via either sole contraction or worsening of sole adhesion to the substratum. To determine whether DA decreases the locomotion rate via sole contraction and to enhance this effect, large snails (n = 17) were injected with high doses of DA (5-11 [micro]g [g.sup.-1] of body weight). In all snails, this injection caused significant contraction of the sole within a few seconds and partial withdrawal of the snail into its shell (Fig. 5A). Sole area ranged from one-third to one-fifth as large as the shell orifice. Such strongly contracted sole area was never observed under normal conditions. The contracted sole was observed for more than 1 h. Under control conditions, injection of physiological saline also resulted in a partial withdrawal of snails (n = 17) into their shells (Fig. 5B). However, the sole area remained equal to the shell orifice that may be observed under normal conditions. Most of these snails (n = 16) recovered normal locomotion within 1-7 min after injection, while one snail was motionless for hours. During restored crawling, sole length and snail speed measurements and the linear relationship between these two variables were very similar to those recorded before injection. Ascorbic acid had no influence on sole length and locomotion rate in either set of experiments.
Thus, DA reliably contracts the sole and, consequently, slows the locomotion rate.
Exposure to [10.sup.-5] mol [l.sup.-1] ergometrine stimulates continuous gliding
All small snails (n = 18 in three experiments) exposed to [10.sup.-5] mol [l.sup.-1] ergometrine demonstrated long, continuous gliding (Fig. 6). Gliding was intermittent in the same number of snails exposed to [10.sup.-6] mol [l.sup.-1] ergometrine, other concentrations, and water.
Ergometrine elongates the sole and, at high concentrations or doses, increases snail speed
The effect of ergometrine on snail sole length and snail speed is shown in Figure 7A. Ten minutes after exposure to ergometrine, the snail increased its sole length and speed proportionally. Mean values showed that the sole was longer ([x.sup.2]-test, P < 0.001, Fig. 7B) and the snail speed was faster ([x.sup.2]-test, P < 0.001, Fig. 7C) in snails (n = 9) exposed to ergometrine when compared to normal conditions.
A similar effect was also found in large snails (n = 7) injected with doses of ergometrine ranging from 0.04 to 0.004 [micro]g [g.sup.-1] of body weight, which approximately cone-sponded to 10-7-[10.sup.-8] mol [1.sup.-1] (Fig. 8). The effect appeared a few minutes after the injection and was observed for 20-30 min. The locomotion rates and sole lengths then slowly returned to those recorded under normal conditions. For large snails, mean values (% [+ or -] S.D.) of the sole length and snail speed and the statistical data were similar to those of the small snails (Fig. 7B, C).
An unexpected result was observed when snails (n = 5) were injected with a dose of ergometrine of 0.0004 [micro]g [g.sup.-1] of body weight (approximately [10.sup.-9] mol [1.sup.-1]). This dose significantly relaxed the sole and was accompanied by long-lasting, slow locomotion of 0.01-0.03 mm [s.sup.-1] (Fig. 8).
The data obtained here demonstrate that 5-HT, DA, and ergometrine modify the relationship between sole length and gliding rate in Lymnaea stagnalis in the same way as in Helix lucorum (Pavlova, 2001). We assume that these effects in L. stagnalis are determined by changes in the number or contraction force of the muscle cells involved in locomotory waves as previously shown in H. lucorum (Pavlova, 2001).
Role of 5-1-IT in gliding rate
In L. stagnalis, 5-HT stimulates gliding (Syed et al., 1988) and increases crawling speed via an apparent increase in the number of muscle cells involved in locomotory waves such as in H. lucorum (Pavlova, 2001). This is exactly the mechanism that provides a dose-dependent increase in locomotor activity in L. stagnalis (Syed et al., 1988; Pavlova, 1997, 2006, 2010). The muscle cells of the horizontal muscular system (Plesch et al., 1975; Bakeeva et al., 1992) and serotonergic axons occupy the same area in the foot sole of L. stagnalis and have synaptic connections (MaKenzie et al., 1998).
Spontaneous shifts of the linear relationship between sole length and snail speed have never been observed under normal conditions (Pavlova, 1990, 1997). In nature, the concentration of biogenic amines in the central nervous system of L. stagnalis depends on seasonal factors (Hetherington et al., 1994). L. stagnalis snails crawl two times slower in autumn than snails of the same size in summer under the same conditions. Autumn snails shift the plots of the linear relationship down along the axis of snail speed (Pavlova. 1990). Hungry pond snails are also known to increase 5-HT concentration in pedal locomotor neurons (Hemadi et al., 2004) and to increase locomotor activity (Bovbjerg, 1965).
Thus, 5-HT "switches on" locomotion but has no direct effect on the tonus of the sole smooth muscles and is not involved in controlling the locomotion rate during a locomotor episode. 5-HT determines the location of the linear relationship plot for each locomotor episode according to the physiological state of the snail; that is, the plots will be shifted upward in hungry summer snails and downward in satiated autumn snails. In a snail, these plots are represented by a set of curves (Fig. 9A) and are distinguished from one another by the number of muscle cells involved in locomotory waves and not by the contraction force of these muscle cells (Fig. 9B) or muscular wave frequency (Pavlova, 2001).
Role of DA in gliding and ergometrine effect
In L. stagnalis, DA causes tonic contraction of longitudinal sole muscle cells, which apparently results in a corresponding decrease in the contraction force of locomotory muscular waves as previously observed in H. lucorum (Pavlova, 2001). When the sole in L. stagnalis is too short to generate muscular waves, one may observe ciliary locomotion (Fig. 4A) that is always slow (Pavlova, 2010). DA contracts the somatic posture muscles in the pteropod mollusc Clione limacina, whereas ergometrine relaxes these muscles (Salcharov and Kabotyansky, 1986).
Ergometrine also relaxes the muscle cells in the sole ot L. stagnalis. High doses of ergometrine disinhibit locomotory muscular waves in L. stagnalis as they do in Helix (Sakharov and Salanki, 1982; Pavlova, 2001). These two effects, muscular wave generation and sole extension, shift the points along a plot of the linear relationship of sole length and snail speed to the right and up (Fig. 7A). They also determine the dose-dependent increase in locomotor activity in isolated soles (Pavlova, 2010). However, low ergometrine doses elongated the sole but were below the threshold for stimulating locomotory muscular waves. In this case, the linear relationship between the elongated sole and slow locomotion was not observed. It was ciliary gliding.
Thus, during locomotor episodes, DA regulates locomotion rates by controlling sole muscle tonus (Fig. 9C) and, consequently, the contraction force of muscle cells involved in locomotory waves (Fig. 9D).
Neurotransmitters in locomotor control (ascertained and putative)
It is possible that yet another transmitter could exist that acts as a DA antagonist and would act similar to ergometrine by elongating the sole and proportionally increasing snail speed. The balance between DA and this unknown neurotransmitter could regulate the sole length at any moment during a locomotor episode and, as a result, control locomotion rate. This neurotransmitter may belong, for instance, to the family of pedal peptides. Pedal peptides are involved in foot relaxation in Aplysia californica (Hall and Lloyd, 1990). They have also been shown to increase locomotor activity in Tritonia diomedea, and are found in the pedal ganglia and foot of L. stagnalis (Willows et al., 1997, 1998) and H. aspersa (Pavlova and Willows, 2005).
DA is not a neurotransmitter that switches locomotion off, because L. stagnalis can be motionless with a rather long sole. Such a neurotransmitter may belong to the MIP (Mytilus inhibitory peptide) family in molluscs (Hirata et al., 1988., Li et al., 1996). L. stagnalis possesses many MT-containing neurons in the pedal ganglia and fibers in the foot (Elekes et al., 2000). DA and MIPs can function as co-transmitters since cessations of locomotion are usually observed when the sole is short, as shown in Figures 3A and 8 and previously (Pavlova, 1990). RPeD1, a right pedal dopamine neuron, contains both DA and an MIP, and can apparently induce the withdrawal reflex (Elekes et al., 2000).
nus, we suppose mat, In L. stagnates, tour neurotransmitters regulate gliding by controlling the states of phasic smooth muscles in the sole. These four neurotransmitters likely interact within the CNS since the foot of L. stagnalis receives pathways originating in the ganglia (McKenzie et al., 1987) and does not have peripheral neuron somata (Zylstra, 1972; McKenzie et al., 1998).
5-HT stimulates the beating of motionless cilia in the sole of L. stagnalis (Syed et al., 1988). The frequency of ciliary beats remained unchanged even when locomotor activity changed significantly (Pavlova, 2010). The mechanism correlating locomotor activity and ciliary stroke amplitude has been previously described (Pavlova and Bakeeva, 1993). The control of ciliary beating in the sole of L. stagnalis will be described in a later report.
Recently, we were far from understanding how L. stag-nalis controls its gliding rate. Now we know that sole muscles may be involved in gliding and controlling the gliding rate, and that this control may coincide with control of the states of the phasic sole muscles.
We think that this control via the modifications of the linear relationship shown here and the corresponding changes to muscular locomotory waves as previously described for H. lucoruni (Pavlova, 2001) is the basic principle for other phasic smooth muscles in vertebrates and invertebrates. Neurotransmitters and hormones involved in the control of different phasic smooth muscles may be different, however. Our findings may be useful for future studies of individual smooth muscles or of co-operative functions between smooth muscles and ciliated epithelium. For instance, in the Fallopian tube and oviducts, the overwhelming majority of investigations focus on ciliary beating while the muscular role of pushing ova through the tube remains unclear (Muglia et al., 1997).
This study was supported by the Russian Foundation for Basic Research, project no. 13-04-01052.
Reference: Biol. Bull. 225: 184-193. (December 2013) [c] 2013 Marine Biological Laboratory
Received 27 February 2012; accepted 23 October 2013. * Address for correspondence: email@example.com
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GALINA A. PAVLOVA
A. N. Belozersky Institute of Physico-Chemical Biology, M. V. LOMOTIOSOV Moscow State University, Moscow 119992, Russia
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|Author:||Pavlova, Galina A.|
|Publication:||The Biological Bulletin|
|Date:||Dec 1, 2013|
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