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. 2010 Apr 6;7 Suppl 2(Suppl 2):S179-91.
doi: 10.1098/rsif.2009.0491.focus. Epub 2010 Jan 13.

Biophysics of magnetic orientation: strengthening the interface between theory and experimental design

Joseph L Kirschvink  1 , Michael Winklhofer, Michael M Walker
Affiliations

Biophysics of magnetic orientation: strengthening the interface between theory and experimental design

Joseph L Kirschvink et al. J R Soc Interface. .

Abstract

The first demonstrations of magnetic effects on the behaviour of migratory birds and homing pigeons in laboratory and field experiments, respectively, provided evidence for the longstanding hypothesis that animals such as birds that migrate and home over long distances would benefit from possession of a magnetic sense. Subsequent identification of at least two plausible biophysical mechanisms for magnetoreception in animals, one based on biogenic magnetite and another on radical-pair biochemical reactions, led to major efforts over recent decades to test predictions of the two models, as well as efforts to understand the ultrastructure and function of the possible magnetoreceptor cells. Unfortunately, progress in understanding the magnetic sense has been challenged by: (i) the availability of a relatively small number of techniques for analysing behavioural responses to magnetic fields by animals; (ii) difficulty in achieving reproducible results using the techniques; and (iii) difficulty in development and implementation of new techniques that might bring greater experimental power. As a consequence, laboratory and field techniques used to study the magnetic sense today remain substantially unchanged, despite the huge developments in technology and instrumentation since the techniques were developed in the 1950s. New methods developed for behavioural study of the magnetic sense over the last 30 years include the use of laboratory conditioning techniques and tracking devices based on transmission of radio signals to and from satellites. Here we consider methodological developments in the study of the magnetic sense and present suggestions for increasing the reproducibility and ease of interpretation of experimental studies. We recommend that future experiments invest more effort in automating control of experiments and data capture, control of stimulation and full blinding of experiments in the rare cases where automation is impossible. We also propose new experiments to confirm whether or not animals can detect magnetic fields using the radical-pair effect together with an alternate hypothesis that may explain the dependence on light of responses by animals to magnetic field stimuli.

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Figures

Figure 1.
Figure 1.
A simple circuit for introducing blind conditions in experiments using static or low-frequency magnetic fields, adapted from Kirschvink (1992b). When building the coil systems, wrap them carefully with two identical strands of wire, placed adjacent to each other and held firmly in place with high-conductivity thermal epoxy (to minimize vibration). These ‘double-wrapped’ coils can then be configured with a silent DPDT switch that will allow the current to flow in series through the two coils, but permits the direction of flow to be reversed in one of them. (a) Circuit with the DPDT switch set so that the current in the two coils is in opposition, yielding no external magnetic field (sham mode). (b) Same circuit with the switch set to produce parallel current flow, yielding the external magnetic field (active mode). We recommend using quasi-random Gellermann (1933) orders to set the active/sham states by a person external to the experiment. If that is impractical, a second DPDT switch can be inserted in the circuit, and two separate investigators can each control one of the switches with separate random orders to ensure fully blinded experimental conditions. Recommendations for multiple-coil designs to produce uniform magnetic stimuli within an experimental chamber are also given by Kirschvink (1992b).
Figure 2.
Figure 2.
Suggestion for implementing a fully blind protocol on behavioural experiments involving both the static geomagnetic field and RF fields, adapted from the experimental protocol of Ritz et al. (2004). (a–c) The orientations of the antenna that were used by Ritz et al. (2004); the RF antenna is in red and the direction of the local geomagnetic field is shown in blue. The position of the RF antenna loop and the power setting on the RF generator (located immediately adjacent to the experimental chamber) are different in each condition (control or ‘sham’). Macroscopic differences other than RF parameters among various test conditions can be eliminated by replacing the mobile loop of coaxial cable with three identical loops fixed in the desired positions, and then using a remote switch to determine which coil is energized. (d) The alternative situation with three fixed loops centred on the bird's cage with a remote switch near the RF generator used to select one of the coils. (e) A method for silently shorting out the RF field using a small reed relay, activated by an external control box. The method is to short across the 2 cm stretch of the outer conductor (the ‘screen’) that is removed on the far side of the RF feed, thereby yielding no RF output for the control or sham. This allows the power output on the RF generator to be run at exactly the same levels for all experiments. By implementing these measures, experimental conditions would not be obvious to the investigators in the room, which otherwise could possibly affect the animals.
Figure 3.
Figure 3.
Logical information flow diagrams for the axially symmetric, blue-light-activated, RF-inhibited migratory magnetic compass response observed in European robins and studied by Ritz et al. (2004). Boxes on the left indicate the primary receptor cells that transduce the indicated stimulus into a coded stream of action potentials. These are usually processed locally, then sent via the major sensory nerve bundles and intermediary ganglia to the brain, represented here by simplified logic gates. The AND gate is a logical construction that passes information (left to right) only if both of the two inputs are true, and the bubble is the standard symbol for an inverted signal. (True becomes false and vice versa; true/false in this context means receiving/lacking streams of action potentials from the receptor cells, indicating the presence/absence of the appropriate activating cue.) (a) Logical flow diagram for the hypothesized radical-pair magnetic compass. (b) Similar logical flow diagram for an axial, magnetite-based compass.
Figure 4.
Figure 4.
Geomagnetic field intensity (in µT) during European climax of (a) the Laschamp magnetic excursion and (b) the last geomagnetic reversal (Brunhes/Matsuyama). The snapshots for the indicated times were computed from the spherical harmonic coefficients provided in Leonhardt et al. (2009) and Leonhardt & Fabian (2007), respectively. The indicated times are in thousands of years (Kyr) before present. (a) At the climax of the excursion, the field in Europe was generally less than < 4 µT with values as low as 2 µT along the southwestern bird migration corridor to Morocco (Northwest Africa). (b) This situation is similar to that of the last geomagnetic reversal, at the climax of which Europe experienced fields generally weaker than 4 µT. These periods of very low field strength last of the order of a few centuries (see also electronic supplementary material).
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