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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.


Merritt coil system for 3D control of magnetic fields.To expose worms to controlled and homogeneous earth-strength magnetic fields we constructed a triple magnetic Merritt coil system (Merritt et al., 1983). (A) Each system creates a magnetic field along the x (i), y (ii), and z (iii) directions and consists of four 1-m2 squares, each arranged orthogonal to the other two. The system generates magnetic and electric fields. To prevent electric fields from affecting our experiments we built a Faraday cage around the experimental volume (iv). Dedicated DC power supplies for each coil (v) allowed us to control the orientation and the magnitude of the net magnetic field within the coil system. Assay plates (vi) were then placed inside the coil system for testing. We empirically calibrated the field within the coil system with the aid of a milligausmeter (vii) from AlphaLab Inc. (Utah, USA). (B) In each magnetic coil system experiment, the north direction of the imposed magnetic field is signified by the 0° on the top of the circular plot. Directly beneath this, and inside the circular plot, the strain's genetic background or geographic origin is indicated. The solid circular histograms represent the heading of the tested populations in a circle where the radius equals 10% of the entire population. Well-fed animals are represented by the black contour, while starved worms are represented by the grey contour. Circular plots had 18 bins (20° each). Similarly, the black and grey arrows represent the mean heading vector for the well-fed and starved populations respectively. The length of the vector is 0 if the population of animals migrated at random, and it is 1 if all animals migrate to a single point. The brown and green dashed curves indicate the heading that would result in (respectively) downward or upward translation at the original isolation site of each strain.DOI:http://dx.doi.org/10.7554/eLife.07493.004
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fig1s1: Merritt coil system for 3D control of magnetic fields.To expose worms to controlled and homogeneous earth-strength magnetic fields we constructed a triple magnetic Merritt coil system (Merritt et al., 1983). (A) Each system creates a magnetic field along the x (i), y (ii), and z (iii) directions and consists of four 1-m2 squares, each arranged orthogonal to the other two. The system generates magnetic and electric fields. To prevent electric fields from affecting our experiments we built a Faraday cage around the experimental volume (iv). Dedicated DC power supplies for each coil (v) allowed us to control the orientation and the magnitude of the net magnetic field within the coil system. Assay plates (vi) were then placed inside the coil system for testing. We empirically calibrated the field within the coil system with the aid of a milligausmeter (vii) from AlphaLab Inc. (Utah, USA). (B) In each magnetic coil system experiment, the north direction of the imposed magnetic field is signified by the 0° on the top of the circular plot. Directly beneath this, and inside the circular plot, the strain's genetic background or geographic origin is indicated. The solid circular histograms represent the heading of the tested populations in a circle where the radius equals 10% of the entire population. Well-fed animals are represented by the black contour, while starved worms are represented by the grey contour. Circular plots had 18 bins (20° each). Similarly, the black and grey arrows represent the mean heading vector for the well-fed and starved populations respectively. The length of the vector is 0 if the population of animals migrated at random, and it is 1 if all animals migrate to a single point. The brown and green dashed curves indicate the heading that would result in (respectively) downward or upward translation at the original isolation site of each strain.DOI:http://dx.doi.org/10.7554/eLife.07493.004

Mentions: Most animals determine the up and down direction by sensing the gravitational field of the earth (e.g., protozoans: Roberts, 2010; crustaceans: Cohen, 1955; vertebrates: Popper and Lu, 2000). Alternatively, magnetotactic bacteria have been shown to use the earth's magnetic field to migrate up or down within the water column (Blakemore, 1975). To help distinguish magnetotactic vs gravitactic mechanisms we built a magnetic coil system capable of producing homogeneous magnetic fields of any desired 3D orientation (Figure 1—figure supplement 1). Our magnetic coil system is comprised of three independently-powered, orthogonal Merritt coil systems that allow the generation of magnetic fields of up to 3× earth strength (Figure 1—figure supplement 1, Merritt et al., 1983). Within the 1-m3 coil system, a smaller 20-cm2 Faraday cage, made with copper fabric, protects the test volume from the electric field that is concomitantly created alongside the magnetic field. Though often ignored in studies on animal magnetic orientation, this precaution was necessary because C. elegans and other animals exhibit strong behavioral responses to electric fields (Gabel et al., 2007; Manière et al., 2011). We repeated our vertical burrowing assay with an artificial magnetic field of earth-strength oriented opposite to the local earth's magnetic field (i.e., magnetic north pointing up rather than the natural orientation where magnetic north points down, Figure 1C). Under these conditions, we expected that worms responding to gravitational cues would continue to migrate down, while worms responding to magnetic cues would reverse their direction and now migrate up. Consistent with magnetic stimuli dictating vertical migration we found that starved N2 strain worms reversed their burrowing behavior and migrated up (Figure 1B red bar).


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)

Merritt coil system for 3D control of magnetic fields.To expose worms to controlled and homogeneous earth-strength magnetic fields we constructed a triple magnetic Merritt coil system (Merritt et al., 1983). (A) Each system creates a magnetic field along the x (i), y (ii), and z (iii) directions and consists of four 1-m2 squares, each arranged orthogonal to the other two. The system generates magnetic and electric fields. To prevent electric fields from affecting our experiments we built a Faraday cage around the experimental volume (iv). Dedicated DC power supplies for each coil (v) allowed us to control the orientation and the magnitude of the net magnetic field within the coil system. Assay plates (vi) were then placed inside the coil system for testing. We empirically calibrated the field within the coil system with the aid of a milligausmeter (vii) from AlphaLab Inc. (Utah, USA). (B) In each magnetic coil system experiment, the north direction of the imposed magnetic field is signified by the 0° on the top of the circular plot. Directly beneath this, and inside the circular plot, the strain's genetic background or geographic origin is indicated. The solid circular histograms represent the heading of the tested populations in a circle where the radius equals 10% of the entire population. Well-fed animals are represented by the black contour, while starved worms are represented by the grey contour. Circular plots had 18 bins (20° each). Similarly, the black and grey arrows represent the mean heading vector for the well-fed and starved populations respectively. The length of the vector is 0 if the population of animals migrated at random, and it is 1 if all animals migrate to a single point. The brown and green dashed curves indicate the heading that would result in (respectively) downward or upward translation at the original isolation site of each strain.DOI:http://dx.doi.org/10.7554/eLife.07493.004
© Copyright Policy
Related In: Results  -  Collection

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

fig1s1: Merritt coil system for 3D control of magnetic fields.To expose worms to controlled and homogeneous earth-strength magnetic fields we constructed a triple magnetic Merritt coil system (Merritt et al., 1983). (A) Each system creates a magnetic field along the x (i), y (ii), and z (iii) directions and consists of four 1-m2 squares, each arranged orthogonal to the other two. The system generates magnetic and electric fields. To prevent electric fields from affecting our experiments we built a Faraday cage around the experimental volume (iv). Dedicated DC power supplies for each coil (v) allowed us to control the orientation and the magnitude of the net magnetic field within the coil system. Assay plates (vi) were then placed inside the coil system for testing. We empirically calibrated the field within the coil system with the aid of a milligausmeter (vii) from AlphaLab Inc. (Utah, USA). (B) In each magnetic coil system experiment, the north direction of the imposed magnetic field is signified by the 0° on the top of the circular plot. Directly beneath this, and inside the circular plot, the strain's genetic background or geographic origin is indicated. The solid circular histograms represent the heading of the tested populations in a circle where the radius equals 10% of the entire population. Well-fed animals are represented by the black contour, while starved worms are represented by the grey contour. Circular plots had 18 bins (20° each). Similarly, the black and grey arrows represent the mean heading vector for the well-fed and starved populations respectively. The length of the vector is 0 if the population of animals migrated at random, and it is 1 if all animals migrate to a single point. The brown and green dashed curves indicate the heading that would result in (respectively) downward or upward translation at the original isolation site of each strain.DOI:http://dx.doi.org/10.7554/eLife.07493.004
Mentions: Most animals determine the up and down direction by sensing the gravitational field of the earth (e.g., protozoans: Roberts, 2010; crustaceans: Cohen, 1955; vertebrates: Popper and Lu, 2000). Alternatively, magnetotactic bacteria have been shown to use the earth's magnetic field to migrate up or down within the water column (Blakemore, 1975). To help distinguish magnetotactic vs gravitactic mechanisms we built a magnetic coil system capable of producing homogeneous magnetic fields of any desired 3D orientation (Figure 1—figure supplement 1). Our magnetic coil system is comprised of three independently-powered, orthogonal Merritt coil systems that allow the generation of magnetic fields of up to 3× earth strength (Figure 1—figure supplement 1, Merritt et al., 1983). Within the 1-m3 coil system, a smaller 20-cm2 Faraday cage, made with copper fabric, protects the test volume from the electric field that is concomitantly created alongside the magnetic field. Though often ignored in studies on animal magnetic orientation, this precaution was necessary because C. elegans and other animals exhibit strong behavioral responses to electric fields (Gabel et al., 2007; Manière et al., 2011). We repeated our vertical burrowing assay with an artificial magnetic field of earth-strength oriented opposite to the local earth's magnetic field (i.e., magnetic north pointing up rather than the natural orientation where magnetic north points down, Figure 1C). Under these conditions, we expected that worms responding to gravitational cues would continue to migrate down, while worms responding to magnetic cues would reverse their direction and now migrate up. Consistent with magnetic stimuli dictating vertical migration we found that starved N2 strain worms reversed their burrowing behavior and migrated up (Figure 1B red bar).

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.