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Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.

Vidal-Gadea A, Ward K, Beron C, Ghorashian N, Gokce S, Russell J, Truong N, Parikh A, Gadea O, Ben-Yakar A, Pierce-Shimomura J - Elife (2015)

Bottom Line: Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair.Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input.C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States.

ABSTRACT
Many organisms spanning from bacteria to mammals orient to the earth's magnetic field. For a few animals, central neurons responsive to earth-strength magnetic fields have been identified; however, magnetosensory neurons have yet to be identified in any animal. We show that the nematode Caenorhabditis elegans orients to the earth's magnetic field during vertical burrowing migrations. Well-fed worms migrated up, while starved worms migrated down. Populations isolated from around the world, migrated at angles to the magnetic vector that would optimize vertical translation in their native soil, with northern- and southern-hemisphere worms displaying opposite migratory preferences. Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair. Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input. C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

No MeSH data available.


Related in: MedlinePlus

Testing the presence of temperature gradients.To determine if the artificial magnetic fields introduced unwanted temperature gradients in our assay we used high-accuracy thermometers capable of measuring 1/100 of a degree Celcius. (A) We recorded the temperature inside the coil system at the edge of the assay plate (where worms were tallied), and at the center of the assay plate (where worms began the experiment). We took temperature measurements under two magnetic regiments: when the earth's magnetic field was actively cancelled out inside the cage (0.000 Gauss, blue), and when we created an artificial magnetic field of earth strength inside the cage (0.650 Gauss, red). (B) The temperature difference between the center and the edge of the plate was reported every 5 min for 30 min before powering the cage on; every 10 min for an hour while the cage was on; and every 5 min for 30 min after powering down the cage. A two-way repeated measures ANOVA failed to reveal significant differences between both treatments (p = 0.123). (C) We measured the temperature difference between the end points of our magnet assays. Two temperature probes were placed at the target zones of magnet assay plates in the absence of a test magnet (blue), or when a magnet was present above one of the two test areas (red). (D) We report the difference between both temperature probes every 10 min for 1 hr. A two-way repeated measures ANOVA failed to find a significant difference between the two experimental conditions (p = 0.559). (E) To empirically confirm that both probes were accurately calibrated we placed them inside a beaker containing 1 l of dH2O and compared their readings between experiments. (F) Throughout our experiments both probes remained in agreement within 1/100th of a degree Celsius. In all experiments the two probes were positioned 5 cm apart.DOI:http://dx.doi.org/10.7554/eLife.07493.006
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fig2s1: Testing the presence of temperature gradients.To determine if the artificial magnetic fields introduced unwanted temperature gradients in our assay we used high-accuracy thermometers capable of measuring 1/100 of a degree Celcius. (A) We recorded the temperature inside the coil system at the edge of the assay plate (where worms were tallied), and at the center of the assay plate (where worms began the experiment). We took temperature measurements under two magnetic regiments: when the earth's magnetic field was actively cancelled out inside the cage (0.000 Gauss, blue), and when we created an artificial magnetic field of earth strength inside the cage (0.650 Gauss, red). (B) The temperature difference between the center and the edge of the plate was reported every 5 min for 30 min before powering the cage on; every 10 min for an hour while the cage was on; and every 5 min for 30 min after powering down the cage. A two-way repeated measures ANOVA failed to reveal significant differences between both treatments (p = 0.123). (C) We measured the temperature difference between the end points of our magnet assays. Two temperature probes were placed at the target zones of magnet assay plates in the absence of a test magnet (blue), or when a magnet was present above one of the two test areas (red). (D) We report the difference between both temperature probes every 10 min for 1 hr. A two-way repeated measures ANOVA failed to find a significant difference between the two experimental conditions (p = 0.559). (E) To empirically confirm that both probes were accurately calibrated we placed them inside a beaker containing 1 l of dH2O and compared their readings between experiments. (F) Throughout our experiments both probes remained in agreement within 1/100th of a degree Celsius. In all experiments the two probes were positioned 5 cm apart.DOI:http://dx.doi.org/10.7554/eLife.07493.006

Mentions: Our above results indicated that C. elegans might be able to detect and orient to magnetic fields of earth strength. To further investigate how worms respond to magnetic fields we placed them at the center of an agar plate and in turn placed this at the center of our 1-m3 Merritt coil system (Figure 1—figure supplement 1; Figure 2A,B). We placed an anesthetic (NaN3) around the circumference of the plate, which allowed us to immobilize and tally worms after they arrived at the plate's periphery. To determine if the coil system generated an unwanted temperature gradient, we measured temperatures across the assay plate in response to a magnetic field (Figure 2—figure supplement 1A,B). Temperature gradients between the assay's start position (at the center of the plate) and the finish position (at its edge) were negligible across time, and did not vary significantly whether we imposed a magnetic field of one earth strength, or if we cancelled out the earth's field by imposing a field of equal strength but opposite direction (two-way repeated measures ANOVA, N = 5, p = 0.123).10.7554/eLife.07493.005Figure 2.Preferred magnetotaxis orientation to a spatially uniform, earth-strength field depends on satiation state, and local field properties.


Magnetosensitive neurons mediate geomagnetic orientation in Caenorhabditis elegans.

Vidal-Gadea A, Ward K, Beron C, Ghorashian N, Gokce S, Russell J, Truong N, Parikh A, Gadea O, Ben-Yakar A, Pierce-Shimomura J - Elife (2015)

Testing the presence of temperature gradients.To determine if the artificial magnetic fields introduced unwanted temperature gradients in our assay we used high-accuracy thermometers capable of measuring 1/100 of a degree Celcius. (A) We recorded the temperature inside the coil system at the edge of the assay plate (where worms were tallied), and at the center of the assay plate (where worms began the experiment). We took temperature measurements under two magnetic regiments: when the earth's magnetic field was actively cancelled out inside the cage (0.000 Gauss, blue), and when we created an artificial magnetic field of earth strength inside the cage (0.650 Gauss, red). (B) The temperature difference between the center and the edge of the plate was reported every 5 min for 30 min before powering the cage on; every 10 min for an hour while the cage was on; and every 5 min for 30 min after powering down the cage. A two-way repeated measures ANOVA failed to reveal significant differences between both treatments (p = 0.123). (C) We measured the temperature difference between the end points of our magnet assays. Two temperature probes were placed at the target zones of magnet assay plates in the absence of a test magnet (blue), or when a magnet was present above one of the two test areas (red). (D) We report the difference between both temperature probes every 10 min for 1 hr. A two-way repeated measures ANOVA failed to find a significant difference between the two experimental conditions (p = 0.559). (E) To empirically confirm that both probes were accurately calibrated we placed them inside a beaker containing 1 l of dH2O and compared their readings between experiments. (F) Throughout our experiments both probes remained in agreement within 1/100th of a degree Celsius. In all experiments the two probes were positioned 5 cm apart.DOI:http://dx.doi.org/10.7554/eLife.07493.006
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4525075&req=5

fig2s1: Testing the presence of temperature gradients.To determine if the artificial magnetic fields introduced unwanted temperature gradients in our assay we used high-accuracy thermometers capable of measuring 1/100 of a degree Celcius. (A) We recorded the temperature inside the coil system at the edge of the assay plate (where worms were tallied), and at the center of the assay plate (where worms began the experiment). We took temperature measurements under two magnetic regiments: when the earth's magnetic field was actively cancelled out inside the cage (0.000 Gauss, blue), and when we created an artificial magnetic field of earth strength inside the cage (0.650 Gauss, red). (B) The temperature difference between the center and the edge of the plate was reported every 5 min for 30 min before powering the cage on; every 10 min for an hour while the cage was on; and every 5 min for 30 min after powering down the cage. A two-way repeated measures ANOVA failed to reveal significant differences between both treatments (p = 0.123). (C) We measured the temperature difference between the end points of our magnet assays. Two temperature probes were placed at the target zones of magnet assay plates in the absence of a test magnet (blue), or when a magnet was present above one of the two test areas (red). (D) We report the difference between both temperature probes every 10 min for 1 hr. A two-way repeated measures ANOVA failed to find a significant difference between the two experimental conditions (p = 0.559). (E) To empirically confirm that both probes were accurately calibrated we placed them inside a beaker containing 1 l of dH2O and compared their readings between experiments. (F) Throughout our experiments both probes remained in agreement within 1/100th of a degree Celsius. In all experiments the two probes were positioned 5 cm apart.DOI:http://dx.doi.org/10.7554/eLife.07493.006
Mentions: Our above results indicated that C. elegans might be able to detect and orient to magnetic fields of earth strength. To further investigate how worms respond to magnetic fields we placed them at the center of an agar plate and in turn placed this at the center of our 1-m3 Merritt coil system (Figure 1—figure supplement 1; Figure 2A,B). We placed an anesthetic (NaN3) around the circumference of the plate, which allowed us to immobilize and tally worms after they arrived at the plate's periphery. To determine if the coil system generated an unwanted temperature gradient, we measured temperatures across the assay plate in response to a magnetic field (Figure 2—figure supplement 1A,B). Temperature gradients between the assay's start position (at the center of the plate) and the finish position (at its edge) were negligible across time, and did not vary significantly whether we imposed a magnetic field of one earth strength, or if we cancelled out the earth's field by imposing a field of equal strength but opposite direction (two-way repeated measures ANOVA, N = 5, p = 0.123).10.7554/eLife.07493.005Figure 2.Preferred magnetotaxis orientation to a spatially uniform, earth-strength field depends on satiation state, and local field properties.

Bottom Line: Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair.Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input.C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

View Article: PubMed Central - PubMed

Affiliation: Department of Neuroscience; Center for Brain, Behavior and Evolution; Center for Learning and Memory; Waggoner Center for Alcohol and Addiction Research; Institute of Cell and Molecular Biology, University of Texas at Austin, Austin, United States.

ABSTRACT
Many organisms spanning from bacteria to mammals orient to the earth's magnetic field. For a few animals, central neurons responsive to earth-strength magnetic fields have been identified; however, magnetosensory neurons have yet to be identified in any animal. We show that the nematode Caenorhabditis elegans orients to the earth's magnetic field during vertical burrowing migrations. Well-fed worms migrated up, while starved worms migrated down. Populations isolated from around the world, migrated at angles to the magnetic vector that would optimize vertical translation in their native soil, with northern- and southern-hemisphere worms displaying opposite migratory preferences. Magnetic orientation and vertical migrations required the TAX-4 cyclic nucleotide-gated ion channel in the AFD sensory neuron pair. Calcium imaging showed that these neurons respond to magnetic fields even without synaptic input. C. elegans may have adapted magnetic orientation to simplify their vertical burrowing migration by reducing the orientation task from three dimensions to one.

No MeSH data available.


Related in: MedlinePlus