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Functional changes in the snail statocyst system elicited by microgravity.

Balaban PM, Malyshev AY, Ierusalimsky VN, Aseyev N, Korshunova TA, Bravarenko NI, Lemak MS, Roshchin M, Zakharov IS, Popova Y, Boyle R - PLoS ONE (2011)

Bottom Line: Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration.A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

View Article: PubMed Central - PubMed

Affiliation: Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia.

ABSTRACT

Background: The mollusk statocyst is a mechanosensing organ detecting the animal's orientation with respect to gravity. This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations.

Methodology/principal findings: In terrestrial gastropod snail we studied the impact of 16- (Foton M-2) and 12-day (Foton M-3) exposure to microgravity in unmanned orbital missions on: (i) the whole animal behavior (Helix lucorum L.), (ii) the statoreceptor responses to tilt in an isolated neural preparation (Helix lucorum L.), and (iii) the differential expression of the Helix pedal peptide (HPep) and the tetrapeptide FMRFamide genes in neural structures (Helix aspersa L.). Experiments were performed 13-42 hours after return to Earth. Latency of body re-orientation to sudden 90° head-down pitch was significantly reduced in postflight snails indicating an enhanced negative gravitaxis response. Statoreceptor responses to tilt in postflight snails were independent of motion direction, in contrast to a directional preference observed in control animals. Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration. A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.

Conclusions/significance: Upregulation of statocyst function in snails following microgravity exposure parallels that observed in vertebrates suggesting fundamental principles underlie gravi-sensing and the organism's ability to adapt to gravity changes. This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

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Postflight changes in directional sensitivity of statocyst response to tilt.A, B: Electrophysiological responses to tilt in statocyst nerve of 4 control and 5 postflight snails (A; Foton M-2) and 8 control and 8 postflight snails (B; Foton M-3) are shown at head down and head up (or tail down) orientations. Scales are expanded in each plot for illustrative purposes. C, D: averaged difference between statocyst nerve responses to tilt corresponding to “head-up” and “head-down” positions are plotted for M-2 (C) and M-3 (D) experiments. A response near zero indicates no directional preference. In both M-2 and M-3 series control and postflight snails the statocyst response demonstrated the opposite directional selectivity. A significant difference between postflight and control snails was observed in the middle portion of tilt in both M-2 and M-3 experiments (p<0.02, RM-ANOVA with Tukey post-hoc analysis).
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pone-0017710-g004: Postflight changes in directional sensitivity of statocyst response to tilt.A, B: Electrophysiological responses to tilt in statocyst nerve of 4 control and 5 postflight snails (A; Foton M-2) and 8 control and 8 postflight snails (B; Foton M-3) are shown at head down and head up (or tail down) orientations. Scales are expanded in each plot for illustrative purposes. C, D: averaged difference between statocyst nerve responses to tilt corresponding to “head-up” and “head-down” positions are plotted for M-2 (C) and M-3 (D) experiments. A response near zero indicates no directional preference. In both M-2 and M-3 series control and postflight snails the statocyst response demonstrated the opposite directional selectivity. A significant difference between postflight and control snails was observed in the middle portion of tilt in both M-2 and M-3 experiments (p<0.02, RM-ANOVA with Tukey post-hoc analysis).

Mentions: In control animals the statocyst response to tilt at 0° orientation (corresponding to snail's head down) was consistently, but not significantly, larger than at 180° (snail's tail down) in both Foton M-2 (Fig. 4A) and M-3 (Fig. 4B) experiments. Responses at 90° and 270° orientations were similar to responses at 0° (data not shown). These results reflect an orientation selectivity of the animal that normally exists and is the basis of negative gravitaxis. But in postflight animals this directionality of statocyst responses to the same tilt stimulus was disturbed. To clearly illustrate this effect, we plotted a difference between the responses obtained at the two opposed orientations (Fig. 4C, D). To make this plot, the average number of spikes of the two responses were subtracted within each preparation and then averaged by group. If no preference to orientation exists, the difference of responses in the plot will be close to zero; and conversely the greater the distance from zero, the more significant is the difference. A significant difference between flight and control snail was observed at several time points for both M-2 (Fig. 4C) and M-3 (Fig. 4D) experiments indicating that responses differed for tilts in the opposite sense (statistical significance was evaluated by repeated measures ANOVA with Tukey post-hoc analysis, p<0.02 for several time points, marked by *). In control snails the statocyst is tuned to ‘head down’ tilt (and more spikes are generated at this orientation), while in postflight snails the directional selectivity was not so clear but tended to be opposite (Fig. 4 B, D). This finding suggests that the neural responses of the statocyst to adequate vestibular stimulation in the postflight snails are independent of the tilt direction, while in the control animals a directional preference for head down tilt occurs.


Functional changes in the snail statocyst system elicited by microgravity.

Balaban PM, Malyshev AY, Ierusalimsky VN, Aseyev N, Korshunova TA, Bravarenko NI, Lemak MS, Roshchin M, Zakharov IS, Popova Y, Boyle R - PLoS ONE (2011)

Postflight changes in directional sensitivity of statocyst response to tilt.A, B: Electrophysiological responses to tilt in statocyst nerve of 4 control and 5 postflight snails (A; Foton M-2) and 8 control and 8 postflight snails (B; Foton M-3) are shown at head down and head up (or tail down) orientations. Scales are expanded in each plot for illustrative purposes. C, D: averaged difference between statocyst nerve responses to tilt corresponding to “head-up” and “head-down” positions are plotted for M-2 (C) and M-3 (D) experiments. A response near zero indicates no directional preference. In both M-2 and M-3 series control and postflight snails the statocyst response demonstrated the opposite directional selectivity. A significant difference between postflight and control snails was observed in the middle portion of tilt in both M-2 and M-3 experiments (p<0.02, RM-ANOVA with Tukey post-hoc analysis).
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Related In: Results  -  Collection

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pone-0017710-g004: Postflight changes in directional sensitivity of statocyst response to tilt.A, B: Electrophysiological responses to tilt in statocyst nerve of 4 control and 5 postflight snails (A; Foton M-2) and 8 control and 8 postflight snails (B; Foton M-3) are shown at head down and head up (or tail down) orientations. Scales are expanded in each plot for illustrative purposes. C, D: averaged difference between statocyst nerve responses to tilt corresponding to “head-up” and “head-down” positions are plotted for M-2 (C) and M-3 (D) experiments. A response near zero indicates no directional preference. In both M-2 and M-3 series control and postflight snails the statocyst response demonstrated the opposite directional selectivity. A significant difference between postflight and control snails was observed in the middle portion of tilt in both M-2 and M-3 experiments (p<0.02, RM-ANOVA with Tukey post-hoc analysis).
Mentions: In control animals the statocyst response to tilt at 0° orientation (corresponding to snail's head down) was consistently, but not significantly, larger than at 180° (snail's tail down) in both Foton M-2 (Fig. 4A) and M-3 (Fig. 4B) experiments. Responses at 90° and 270° orientations were similar to responses at 0° (data not shown). These results reflect an orientation selectivity of the animal that normally exists and is the basis of negative gravitaxis. But in postflight animals this directionality of statocyst responses to the same tilt stimulus was disturbed. To clearly illustrate this effect, we plotted a difference between the responses obtained at the two opposed orientations (Fig. 4C, D). To make this plot, the average number of spikes of the two responses were subtracted within each preparation and then averaged by group. If no preference to orientation exists, the difference of responses in the plot will be close to zero; and conversely the greater the distance from zero, the more significant is the difference. A significant difference between flight and control snail was observed at several time points for both M-2 (Fig. 4C) and M-3 (Fig. 4D) experiments indicating that responses differed for tilts in the opposite sense (statistical significance was evaluated by repeated measures ANOVA with Tukey post-hoc analysis, p<0.02 for several time points, marked by *). In control snails the statocyst is tuned to ‘head down’ tilt (and more spikes are generated at this orientation), while in postflight snails the directional selectivity was not so clear but tended to be opposite (Fig. 4 B, D). This finding suggests that the neural responses of the statocyst to adequate vestibular stimulation in the postflight snails are independent of the tilt direction, while in the control animals a directional preference for head down tilt occurs.

Bottom Line: Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration.A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

View Article: PubMed Central - PubMed

Affiliation: Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow, Russia.

ABSTRACT

Background: The mollusk statocyst is a mechanosensing organ detecting the animal's orientation with respect to gravity. This system has clear similarities to its vertebrate counterparts: a weight-lending mass, an epithelial layer containing small supporting cells and the large sensory hair cells, and an output eliciting compensatory body reflexes to perturbations.

Methodology/principal findings: In terrestrial gastropod snail we studied the impact of 16- (Foton M-2) and 12-day (Foton M-3) exposure to microgravity in unmanned orbital missions on: (i) the whole animal behavior (Helix lucorum L.), (ii) the statoreceptor responses to tilt in an isolated neural preparation (Helix lucorum L.), and (iii) the differential expression of the Helix pedal peptide (HPep) and the tetrapeptide FMRFamide genes in neural structures (Helix aspersa L.). Experiments were performed 13-42 hours after return to Earth. Latency of body re-orientation to sudden 90° head-down pitch was significantly reduced in postflight snails indicating an enhanced negative gravitaxis response. Statoreceptor responses to tilt in postflight snails were independent of motion direction, in contrast to a directional preference observed in control animals. Positive relation between tilt velocity and firing rate was observed in both control and postflight snails, but the response magnitude was significantly larger in postflight snails indicating an enhanced sensitivity to acceleration. A significant increase in mRNA expression of the gene encoding HPep, a peptide linked to ciliary beating, in statoreceptors was observed in postflight snails; no differential expression of the gene encoding FMRFamide, a possible neurotransmission modulator, was observed.

Conclusions/significance: Upregulation of statocyst function in snails following microgravity exposure parallels that observed in vertebrates suggesting fundamental principles underlie gravi-sensing and the organism's ability to adapt to gravity changes. This simple animal model offers the possibility to describe general subcellular mechanisms of nervous system's response to conditions on Earth and in space.

Show MeSH
Related in: MedlinePlus