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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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Negative gravitaxis response in control and postflight snails.A. Phases of the stereotypic response to sudden shift of the snail with platform from horizontal to “head down” position. B. Latency of gravitaxis reaction phases acquired during Foton M-2 experiments. The plot shows averaged (±SEM) time of the behavioral responses at 4 phases of the negative gravitaxis response in 14 flight and 8 control snails. Flight snails were faster in their response to pitch stimulation at each phase, and the difference reach level of significance p<0.05 at the later phases T3 and T4. C. Changes in latency of gravitaxis reaction of T2 phase acquired during Foton M-3 experiments. The plot shows averaged (±SEM) time of the behavioral responses at the T2 phase in 5 flight and 6 control snails tested before (black columns) and after (open columns) flight. Flight snails were faster than control snails as a group in their response to pitch stimulation, insignificant at T1 (not shown) but significant (p<0.02) at T2 phase. Post-flight gravitaxis responses were significantly faster (shorter latency of T2; p<0.04) than pre-flight responses recorded in the same snail.
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pone-0017710-g002: Negative gravitaxis response in control and postflight snails.A. Phases of the stereotypic response to sudden shift of the snail with platform from horizontal to “head down” position. B. Latency of gravitaxis reaction phases acquired during Foton M-2 experiments. The plot shows averaged (±SEM) time of the behavioral responses at 4 phases of the negative gravitaxis response in 14 flight and 8 control snails. Flight snails were faster in their response to pitch stimulation at each phase, and the difference reach level of significance p<0.05 at the later phases T3 and T4. C. Changes in latency of gravitaxis reaction of T2 phase acquired during Foton M-3 experiments. The plot shows averaged (±SEM) time of the behavioral responses at the T2 phase in 5 flight and 6 control snails tested before (black columns) and after (open columns) flight. Flight snails were faster than control snails as a group in their response to pitch stimulation, insignificant at T1 (not shown) but significant (p<0.02) at T2 phase. Post-flight gravitaxis responses were significantly faster (shorter latency of T2; p<0.04) than pre-flight responses recorded in the same snail.

Mentions: Natural stimulation of the statocyst was performed on a custom tilt setup, which was slightly modified for the experiments of Foton M-3 to enhance testing. Figure 1A shows a cartoon of the tilt platform with the isolated neural preparation. In both series of experiments the preparation dish was positioned at 45° or 90° steps to test the statocyst's physiological response at different orientations with respect to gravity. 0° orientation was defined as the position in which rise of the platform (Fig. 1A) mimicked a downward pitch of the animal's head in intact snails (Fig. 1B, middle cartoon), and corresponded to T0 (see Fig. 2A) in the behavioral experiments. Increments in degrees were taken in a counter-clockwise direction, as viewed from above, up to a ‘tail down’ or ‘head-up’ snail tilt of 180° (Fig. 1B, lower cartoon). Platform tilt was pneumatically driven in M-2 experiments, and its direction was controlled by an electronically controlled valve manually switched on/off. To align the platform movements to the precise extracellular signal the start and finish times of tilt were manually tagged. Measured time of platform rise was 1.1 s (peak tilt velocity 17.3°/s), fall was 1 s, and the mid-point of tilt profile was set as time 0 for later analysis. We improved the stimulus paradigm for M-3 experiments by using a microcontroller-operated DC stepper motor with worm gearing to drive the platform tilt. The duration of tilt motion was thereby adjustable, and permitted delivering stimuli with different, but still brief, acceleration phases to ensure a response threshold to tilt was reached. This flexibility in adjusting the test protocol was particularly important in the postflight experiments where differences in threshold and response saturation might occur. We tested 4 different durations of 19° platform rise in the range from 550–3020 ms (6.3–34.5°/s). Angle of platform movement was measured by an in-line potentiometer, whose moving rod was used as the axis of rotation. The potentiometer measures were recorded on a separate channel and the beginning of movement was set as time 0.


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)

Negative gravitaxis response in control and postflight snails.A. Phases of the stereotypic response to sudden shift of the snail with platform from horizontal to “head down” position. B. Latency of gravitaxis reaction phases acquired during Foton M-2 experiments. The plot shows averaged (±SEM) time of the behavioral responses at 4 phases of the negative gravitaxis response in 14 flight and 8 control snails. Flight snails were faster in their response to pitch stimulation at each phase, and the difference reach level of significance p<0.05 at the later phases T3 and T4. C. Changes in latency of gravitaxis reaction of T2 phase acquired during Foton M-3 experiments. The plot shows averaged (±SEM) time of the behavioral responses at the T2 phase in 5 flight and 6 control snails tested before (black columns) and after (open columns) flight. Flight snails were faster than control snails as a group in their response to pitch stimulation, insignificant at T1 (not shown) but significant (p<0.02) at T2 phase. Post-flight gravitaxis responses were significantly faster (shorter latency of T2; p<0.04) than pre-flight responses recorded in the same snail.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3066201&req=5

pone-0017710-g002: Negative gravitaxis response in control and postflight snails.A. Phases of the stereotypic response to sudden shift of the snail with platform from horizontal to “head down” position. B. Latency of gravitaxis reaction phases acquired during Foton M-2 experiments. The plot shows averaged (±SEM) time of the behavioral responses at 4 phases of the negative gravitaxis response in 14 flight and 8 control snails. Flight snails were faster in their response to pitch stimulation at each phase, and the difference reach level of significance p<0.05 at the later phases T3 and T4. C. Changes in latency of gravitaxis reaction of T2 phase acquired during Foton M-3 experiments. The plot shows averaged (±SEM) time of the behavioral responses at the T2 phase in 5 flight and 6 control snails tested before (black columns) and after (open columns) flight. Flight snails were faster than control snails as a group in their response to pitch stimulation, insignificant at T1 (not shown) but significant (p<0.02) at T2 phase. Post-flight gravitaxis responses were significantly faster (shorter latency of T2; p<0.04) than pre-flight responses recorded in the same snail.
Mentions: Natural stimulation of the statocyst was performed on a custom tilt setup, which was slightly modified for the experiments of Foton M-3 to enhance testing. Figure 1A shows a cartoon of the tilt platform with the isolated neural preparation. In both series of experiments the preparation dish was positioned at 45° or 90° steps to test the statocyst's physiological response at different orientations with respect to gravity. 0° orientation was defined as the position in which rise of the platform (Fig. 1A) mimicked a downward pitch of the animal's head in intact snails (Fig. 1B, middle cartoon), and corresponded to T0 (see Fig. 2A) in the behavioral experiments. Increments in degrees were taken in a counter-clockwise direction, as viewed from above, up to a ‘tail down’ or ‘head-up’ snail tilt of 180° (Fig. 1B, lower cartoon). Platform tilt was pneumatically driven in M-2 experiments, and its direction was controlled by an electronically controlled valve manually switched on/off. To align the platform movements to the precise extracellular signal the start and finish times of tilt were manually tagged. Measured time of platform rise was 1.1 s (peak tilt velocity 17.3°/s), fall was 1 s, and the mid-point of tilt profile was set as time 0 for later analysis. We improved the stimulus paradigm for M-3 experiments by using a microcontroller-operated DC stepper motor with worm gearing to drive the platform tilt. The duration of tilt motion was thereby adjustable, and permitted delivering stimuli with different, but still brief, acceleration phases to ensure a response threshold to tilt was reached. This flexibility in adjusting the test protocol was particularly important in the postflight experiments where differences in threshold and response saturation might occur. We tested 4 different durations of 19° platform rise in the range from 550–3020 ms (6.3–34.5°/s). Angle of platform movement was measured by an in-line potentiometer, whose moving rod was used as the axis of rotation. The potentiometer measures were recorded on a separate channel and the beginning of movement was set as time 0.

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