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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

Measuring AFD calcium activity in partially and fully restrained worms.(A) Worm-immobilization chip for high-resolution fluorescence microscopy. The two-level device consists of a valve layer (pink) sitting above a flow layer where the worms reside (grey). Animals enter the immobilization chamber via the worm input as fluid flow is directed to the fluid output. Small channels across the outer edge of the immobilization chamber permit fluid flow to pass but block the passage of the worms (left). As the flow pushes the worms against the outer edge of the chamber the valve layer is pressurized to fully immobilize the worms (right). A magnified view of a single animal pressed against the small channels along the outer edge of the immobilization chamber is shown during immobilization. (B) Alternatively, we partially restrained worms on an agar pad while measuring the brightness of the AFD (or AWC) sensory neurons before, during, and after exposure to a 60-Gauss magnetic stimulus. Images were taken only when the AFD soma was stationary. While consistent with our immobilized-worm experiments in sign (Figure 7), the amplitude of the responses were about 10 times larger in partially restrained animals. (C) Expression of GCaMP3 in AFD neurons did not impair the worm's ability to orient to magnetic fields. * p < 0.05, ** p < 0.001. All values reported are means, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.07493.014
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fig7s1: Measuring AFD calcium activity in partially and fully restrained worms.(A) Worm-immobilization chip for high-resolution fluorescence microscopy. The two-level device consists of a valve layer (pink) sitting above a flow layer where the worms reside (grey). Animals enter the immobilization chamber via the worm input as fluid flow is directed to the fluid output. Small channels across the outer edge of the immobilization chamber permit fluid flow to pass but block the passage of the worms (left). As the flow pushes the worms against the outer edge of the chamber the valve layer is pressurized to fully immobilize the worms (right). A magnified view of a single animal pressed against the small channels along the outer edge of the immobilization chamber is shown during immobilization. (B) Alternatively, we partially restrained worms on an agar pad while measuring the brightness of the AFD (or AWC) sensory neurons before, during, and after exposure to a 60-Gauss magnetic stimulus. Images were taken only when the AFD soma was stationary. While consistent with our immobilized-worm experiments in sign (Figure 7), the amplitude of the responses were about 10 times larger in partially restrained animals. (C) Expression of GCaMP3 in AFD neurons did not impair the worm's ability to orient to magnetic fields. * p < 0.05, ** p < 0.001. All values reported are means, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.07493.014

Mentions: To determine whether the AFD neurons are directly responsive to magnetic fields, we measured the fluorescence of a genetically encoded calcium indicator, GCaMP3, in fully immobilized worms (Figure 7A, and Figure 7—figure supplement 1A). After recording baseline activity (Figure 7B), we exposed mechanically immobilized worms to an 8-s, 65-Gauss (100× earth) rotating (2 Hz) magnetic stimulus (see ‘Materials and methods’ for details). We observed a transient increase in the average brightness of the AFD neurons (Figure 7C). Successive stimuli consistently produced a reduced response (Figure 7D). We observed a similar response when the magnetic stimulus was decreased to 10× and 1× earth stimuli (6.5 and 0.65 Gauss respectively, Figure 7E,F). To help determine if the AFD neurons themselves are magnetosensitive, and not just synaptically downstream from ‘real’ magnetoreceptive neuron(s), we measured AFD calcium responses in worms impaired in rapid and dense-core synaptic transmission (unc-13 and unc-31 mutant strains, Ahmed et al., 1992; Ann et al., 1997). In the absence of chemical synaptic or neuromodulatory inputs, the AFD neurons continued to respond to magnetic fields (Figure 7G,H). Qualitatively similar results (but higher in amplitude) were observed for worms that were partially restrained (Figure 7—figure supplement 1B). Magnetic-induced calcium responses in AFD were not observed in a tax-4 mutant background, suggesting that this requires Ca2+ entering the TAX-4 cGMP-gated ion channel (Figure 7I, Figure 7—figure supplement 1B). Responses were also not observed in an adjacent sensory neuron pair AWC (Figure 7J and Figure 7—figure supplement 1B). To quantitatively compare the magnetosensory response of AFD for different conditions and mutant backgrounds, we plotted the average GCamp3.0 intensity during the final 4 s of the magnetic stimulus relative to a 4-s baseline before presentation of the stimulus (for the no-stimulus control we used the same time window as for the other recordings). We found that the change in brightness was significantly greater than control for all test conditions except in the case of tax-4 mutant background (Figure 7K). Our imaging results provide physiological evidence that the AFD sensory neurons respond to magnetosensory stimuli relevant to geomagnetic orientation.10.7554/eLife.07493.013Figure 7.The AFD sensory neurons respond to magnetic stimuli.


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)

Measuring AFD calcium activity in partially and fully restrained worms.(A) Worm-immobilization chip for high-resolution fluorescence microscopy. The two-level device consists of a valve layer (pink) sitting above a flow layer where the worms reside (grey). Animals enter the immobilization chamber via the worm input as fluid flow is directed to the fluid output. Small channels across the outer edge of the immobilization chamber permit fluid flow to pass but block the passage of the worms (left). As the flow pushes the worms against the outer edge of the chamber the valve layer is pressurized to fully immobilize the worms (right). A magnified view of a single animal pressed against the small channels along the outer edge of the immobilization chamber is shown during immobilization. (B) Alternatively, we partially restrained worms on an agar pad while measuring the brightness of the AFD (or AWC) sensory neurons before, during, and after exposure to a 60-Gauss magnetic stimulus. Images were taken only when the AFD soma was stationary. While consistent with our immobilized-worm experiments in sign (Figure 7), the amplitude of the responses were about 10 times larger in partially restrained animals. (C) Expression of GCaMP3 in AFD neurons did not impair the worm's ability to orient to magnetic fields. * p < 0.05, ** p < 0.001. All values reported are means, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.07493.014
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Related In: Results  -  Collection

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fig7s1: Measuring AFD calcium activity in partially and fully restrained worms.(A) Worm-immobilization chip for high-resolution fluorescence microscopy. The two-level device consists of a valve layer (pink) sitting above a flow layer where the worms reside (grey). Animals enter the immobilization chamber via the worm input as fluid flow is directed to the fluid output. Small channels across the outer edge of the immobilization chamber permit fluid flow to pass but block the passage of the worms (left). As the flow pushes the worms against the outer edge of the chamber the valve layer is pressurized to fully immobilize the worms (right). A magnified view of a single animal pressed against the small channels along the outer edge of the immobilization chamber is shown during immobilization. (B) Alternatively, we partially restrained worms on an agar pad while measuring the brightness of the AFD (or AWC) sensory neurons before, during, and after exposure to a 60-Gauss magnetic stimulus. Images were taken only when the AFD soma was stationary. While consistent with our immobilized-worm experiments in sign (Figure 7), the amplitude of the responses were about 10 times larger in partially restrained animals. (C) Expression of GCaMP3 in AFD neurons did not impair the worm's ability to orient to magnetic fields. * p < 0.05, ** p < 0.001. All values reported are means, and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.07493.014
Mentions: To determine whether the AFD neurons are directly responsive to magnetic fields, we measured the fluorescence of a genetically encoded calcium indicator, GCaMP3, in fully immobilized worms (Figure 7A, and Figure 7—figure supplement 1A). After recording baseline activity (Figure 7B), we exposed mechanically immobilized worms to an 8-s, 65-Gauss (100× earth) rotating (2 Hz) magnetic stimulus (see ‘Materials and methods’ for details). We observed a transient increase in the average brightness of the AFD neurons (Figure 7C). Successive stimuli consistently produced a reduced response (Figure 7D). We observed a similar response when the magnetic stimulus was decreased to 10× and 1× earth stimuli (6.5 and 0.65 Gauss respectively, Figure 7E,F). To help determine if the AFD neurons themselves are magnetosensitive, and not just synaptically downstream from ‘real’ magnetoreceptive neuron(s), we measured AFD calcium responses in worms impaired in rapid and dense-core synaptic transmission (unc-13 and unc-31 mutant strains, Ahmed et al., 1992; Ann et al., 1997). In the absence of chemical synaptic or neuromodulatory inputs, the AFD neurons continued to respond to magnetic fields (Figure 7G,H). Qualitatively similar results (but higher in amplitude) were observed for worms that were partially restrained (Figure 7—figure supplement 1B). Magnetic-induced calcium responses in AFD were not observed in a tax-4 mutant background, suggesting that this requires Ca2+ entering the TAX-4 cGMP-gated ion channel (Figure 7I, Figure 7—figure supplement 1B). Responses were also not observed in an adjacent sensory neuron pair AWC (Figure 7J and Figure 7—figure supplement 1B). To quantitatively compare the magnetosensory response of AFD for different conditions and mutant backgrounds, we plotted the average GCamp3.0 intensity during the final 4 s of the magnetic stimulus relative to a 4-s baseline before presentation of the stimulus (for the no-stimulus control we used the same time window as for the other recordings). We found that the change in brightness was significantly greater than control for all test conditions except in the case of tax-4 mutant background (Figure 7K). Our imaging results provide physiological evidence that the AFD sensory neurons respond to magnetosensory stimuli relevant to geomagnetic orientation.10.7554/eLife.07493.013Figure 7.The AFD sensory neurons respond to magnetic stimuli.

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