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Spontaneous Behaviors and Wall-Curvature Lead to Apparent Wall Preference in Planarian.

Akiyama Y, Agata K, Inoue T - PLoS ONE (2015)

Bottom Line: When we tested another spontaneous behavior, the wigwag movement of the planarian head, using computer simulation with various wigwag angles and wigwag intervals, large wigwag angle and short wigwag interval reduced wall-preference behavior.Furthermore, in accord with this simulation, when we tested planarian wall-preference behavior using several assay fields with different curvature of the wall, we found that concavity and sharp curvature of walls negatively impacted wall preference by affecting the permissible angle of the wigwag movement.Together, these results indicate that planarian wall preference may be involuntarily caused by the combination of two spontaneous planarian behaviors: moving straight ahead until reaching a wall and then moving along it in the absence of environmental cues, and wigwag movements of the head.

View Article: PubMed Central - PubMed

Affiliation: Department of Biophysics, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwake, Sakyo-ku, Kyoto, Japan.

ABSTRACT
The planarian Dugesia japonica tends to stay near the walls of its breeding containers and experimental dishes in the laboratory, a phenomenon called "wall preference". This behavior is thought to be important for environmental adaptation, such as hiding by planarians in nature. However, the mechanisms regulating wall-preference behavior are not well understood, since this behavior occurs in the absence of any particular stimulation. Here we show the mechanisms of wall-preference behavior. Surprisingly, planarian wall-preference behavior was also shown even by the head alone and by headless planarians. These results indicate that planarian "wall-preference" behavior only appears to be a "preference" behavior, and is actually an outcome of spontaneous behaviors, rather than of brain function. We found that in the absence of environmental cues planarians moved basically straight ahead until they reached a wall, and that after reaching a wall, they changed their direction of movement to one tangential to the wall, suggesting that this spontaneous behavior may play a critical role in the wall preference. When we tested another spontaneous behavior, the wigwag movement of the planarian head, using computer simulation with various wigwag angles and wigwag intervals, large wigwag angle and short wigwag interval reduced wall-preference behavior. This indicated that wigwag movement may determine the probability of staying near the wall or leaving the wall. Furthermore, in accord with this simulation, when we tested planarian wall-preference behavior using several assay fields with different curvature of the wall, we found that concavity and sharp curvature of walls negatively impacted wall preference by affecting the permissible angle of the wigwag movement. Together, these results indicate that planarian wall preference may be involuntarily caused by the combination of two spontaneous planarian behaviors: moving straight ahead until reaching a wall and then moving along it in the absence of environmental cues, and wigwag movements of the head.

No MeSH data available.


Related in: MedlinePlus

Wall preference is independent of head function.(A) Trajectories and heat map of planarian wall preference of intact, head-fragment, and headless animals. The central circle indicates the starting region. n = 10, t = 300 sec. (B) Wall-preference index and central-preference index. ***, p < 0.005; **, p < 0.01; in the Wilcoxon signed rank test. (C) Distance moved by intact, head-fragment, and headless animals during assay. ***, p < 0.005 in Student's t-test. (D) Points of detachment from the wall and trajectories of movement of intact, head-fragment, and headless planarians. Red circles indicate the points of detachment from the walls. n = 10. t = 300 sec. (E) The mean time between reaching the wall and detaching from the wall. n = 10. t = 300 sec. ns, not significant in one-way ANOVA.
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pone.0142214.g002: Wall preference is independent of head function.(A) Trajectories and heat map of planarian wall preference of intact, head-fragment, and headless animals. The central circle indicates the starting region. n = 10, t = 300 sec. (B) Wall-preference index and central-preference index. ***, p < 0.005; **, p < 0.01; in the Wilcoxon signed rank test. (C) Distance moved by intact, head-fragment, and headless animals during assay. ***, p < 0.005 in Student's t-test. (D) Points of detachment from the wall and trajectories of movement of intact, head-fragment, and headless planarians. Red circles indicate the points of detachment from the walls. n = 10. t = 300 sec. (E) The mean time between reaching the wall and detaching from the wall. n = 10. t = 300 sec. ns, not significant in one-way ANOVA.

Mentions: Next, to investigate whether wall-preference behavior required brain function, we tested the behavior of intact animals, head fragments, and headless animals in the rectangular field. All individuals of the head fragment and headless groups moved to the wall region (p < 0.001, p < 0.001, respectively, in the χ2 test), similarly to intact planarians (p < 0.001 in the χ2 test) (Fig 2A). The preference index clearly indicated that the planarians showed wall preference regardless of amputation (Fig 2B). Interestingly, we found that the wall-preference index was lower in head fragments and headless animals than in intact animals. Therefore, to evaluate the partial contribution of brain activity to the wall preference, we measured the distance the animals moved during the assay. The results showed that the head fragment and the headless fragment moved a shorter distance than intact animals (Fig 2C), indicating that the wall-preference index might have been affected by the assay conditions rather than by loss of the brain. These results suggest that planarian wall-preference behavior is achieved independently of brain function. Importantly, the trajectories of the planarian movement and the time from reaching the wall until moving away from the wall in the absence of any particular stimulation revealed that all intact planarians, head fragments, and headless planarians sporadically left walls and returned to walls after reaching them, rather than staying at the wall (Fig 2D and 2E). This indicates that planarian does not necessarily continue to stay at the wall.


Spontaneous Behaviors and Wall-Curvature Lead to Apparent Wall Preference in Planarian.

Akiyama Y, Agata K, Inoue T - PLoS ONE (2015)

Wall preference is independent of head function.(A) Trajectories and heat map of planarian wall preference of intact, head-fragment, and headless animals. The central circle indicates the starting region. n = 10, t = 300 sec. (B) Wall-preference index and central-preference index. ***, p < 0.005; **, p < 0.01; in the Wilcoxon signed rank test. (C) Distance moved by intact, head-fragment, and headless animals during assay. ***, p < 0.005 in Student's t-test. (D) Points of detachment from the wall and trajectories of movement of intact, head-fragment, and headless planarians. Red circles indicate the points of detachment from the walls. n = 10. t = 300 sec. (E) The mean time between reaching the wall and detaching from the wall. n = 10. t = 300 sec. ns, not significant in one-way ANOVA.
© Copyright Policy
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4635015&req=5

pone.0142214.g002: Wall preference is independent of head function.(A) Trajectories and heat map of planarian wall preference of intact, head-fragment, and headless animals. The central circle indicates the starting region. n = 10, t = 300 sec. (B) Wall-preference index and central-preference index. ***, p < 0.005; **, p < 0.01; in the Wilcoxon signed rank test. (C) Distance moved by intact, head-fragment, and headless animals during assay. ***, p < 0.005 in Student's t-test. (D) Points of detachment from the wall and trajectories of movement of intact, head-fragment, and headless planarians. Red circles indicate the points of detachment from the walls. n = 10. t = 300 sec. (E) The mean time between reaching the wall and detaching from the wall. n = 10. t = 300 sec. ns, not significant in one-way ANOVA.
Mentions: Next, to investigate whether wall-preference behavior required brain function, we tested the behavior of intact animals, head fragments, and headless animals in the rectangular field. All individuals of the head fragment and headless groups moved to the wall region (p < 0.001, p < 0.001, respectively, in the χ2 test), similarly to intact planarians (p < 0.001 in the χ2 test) (Fig 2A). The preference index clearly indicated that the planarians showed wall preference regardless of amputation (Fig 2B). Interestingly, we found that the wall-preference index was lower in head fragments and headless animals than in intact animals. Therefore, to evaluate the partial contribution of brain activity to the wall preference, we measured the distance the animals moved during the assay. The results showed that the head fragment and the headless fragment moved a shorter distance than intact animals (Fig 2C), indicating that the wall-preference index might have been affected by the assay conditions rather than by loss of the brain. These results suggest that planarian wall-preference behavior is achieved independently of brain function. Importantly, the trajectories of the planarian movement and the time from reaching the wall until moving away from the wall in the absence of any particular stimulation revealed that all intact planarians, head fragments, and headless planarians sporadically left walls and returned to walls after reaching them, rather than staying at the wall (Fig 2D and 2E). This indicates that planarian does not necessarily continue to stay at the wall.

Bottom Line: When we tested another spontaneous behavior, the wigwag movement of the planarian head, using computer simulation with various wigwag angles and wigwag intervals, large wigwag angle and short wigwag interval reduced wall-preference behavior.Furthermore, in accord with this simulation, when we tested planarian wall-preference behavior using several assay fields with different curvature of the wall, we found that concavity and sharp curvature of walls negatively impacted wall preference by affecting the permissible angle of the wigwag movement.Together, these results indicate that planarian wall preference may be involuntarily caused by the combination of two spontaneous planarian behaviors: moving straight ahead until reaching a wall and then moving along it in the absence of environmental cues, and wigwag movements of the head.

View Article: PubMed Central - PubMed

Affiliation: Department of Biophysics, Graduate School of Science, Kyoto University, Kitashirakawa-Oiwake, Sakyo-ku, Kyoto, Japan.

ABSTRACT
The planarian Dugesia japonica tends to stay near the walls of its breeding containers and experimental dishes in the laboratory, a phenomenon called "wall preference". This behavior is thought to be important for environmental adaptation, such as hiding by planarians in nature. However, the mechanisms regulating wall-preference behavior are not well understood, since this behavior occurs in the absence of any particular stimulation. Here we show the mechanisms of wall-preference behavior. Surprisingly, planarian wall-preference behavior was also shown even by the head alone and by headless planarians. These results indicate that planarian "wall-preference" behavior only appears to be a "preference" behavior, and is actually an outcome of spontaneous behaviors, rather than of brain function. We found that in the absence of environmental cues planarians moved basically straight ahead until they reached a wall, and that after reaching a wall, they changed their direction of movement to one tangential to the wall, suggesting that this spontaneous behavior may play a critical role in the wall preference. When we tested another spontaneous behavior, the wigwag movement of the planarian head, using computer simulation with various wigwag angles and wigwag intervals, large wigwag angle and short wigwag interval reduced wall-preference behavior. This indicated that wigwag movement may determine the probability of staying near the wall or leaving the wall. Furthermore, in accord with this simulation, when we tested planarian wall-preference behavior using several assay fields with different curvature of the wall, we found that concavity and sharp curvature of walls negatively impacted wall preference by affecting the permissible angle of the wigwag movement. Together, these results indicate that planarian wall preference may be involuntarily caused by the combination of two spontaneous planarian behaviors: moving straight ahead until reaching a wall and then moving along it in the absence of environmental cues, and wigwag movements of the head.

No MeSH data available.


Related in: MedlinePlus