Conditioning to magnetic directions.

In neurobiology, psychology and sensory physiology, operant conditioning is a valuable tool for gaining access to the sensory world of animals. Conditioning experiments have revealed features of the capacity to detect sensory qualities, such as thresholds, range and the ability to discriminate, and have explored the functional mode of sensory mechanisms, the neuronal pathways and the areas of the brain involved. Our knowledge of the visual and auditory sensitivity of animals is largely based on conditioning experiments. With regard to the sensitivity for the geomagnetic field, the situation is different. Although spontaneous responses of migratory birds and homing pigeons clearly indicated that these animals are sensitive to the geomagnetic field [1], attempts at conditioning largely failed, with the negative results outnumbering the few positive ones. Many neurobiologists have more trust in conditioning experiments, in which responses can be elicited at will, than in spontaneous behavior that occurs only during certain times of the year or in certain conditions. Hence the failure to obtain proper conditioned responses began to undermine the acceptance of magnetoreception in general. Guided by the firm ‘belief’ that ‘we know of no case in which a proven exteroreceptive sensitivity has remained impossible to demonstrate clearly with conditioning techniques’ [2], many neurobiologists questioned the ability of animals to perceive magnetic fields, which, in turn, delayed and still delays the analysis of the neuronal basis of this ability. Efforts to condition animals to magnetic stimuli have been carried out since the 1950s. In the last decades of the 20th century, honey bees and several species of fish could be conditioned to magnetic fields, with new positive results reported recently. In most of these experiments, the stimulus consisted of changes in magnetic intensity and the animals had to discriminate between the absence and the presence of a magnetic anomaly. With birds and mammals, however, similar attempts were largely unsuccessful. Until recently, there was no known case of a mammal successfully conditioned to magnetic stimuli, and occasional positive results reported from birds proved hard to reproduce and were outnumbered by negative results. In particular, in birds this seemed rather odd, given the many positive experiments based on spontaneous behavior: for example, migratory birds prefer directions that correspond to their seasonally appropriate migratory direction under controlled laboratory conditions; when north of the ambient magnetic field is shifted, they change their headings in a corresponding way. This raised general questions about conditioning to magnetic stimuli – why was it so seldom successful? Three possible reasons why traditional conditioning techniques may have failed have been suggested [3]. The first is that a factor like the geomagnetic field, naturally used for spatial tasks in connection with orientation and navigation, might not be easily associated with a food reward, and in the limited space of a laboratory, conditioning to magnetic stimuli might meet constraints of learning. The second possible reason is that, in nature, the geomagnetic field never undergoes any rapid changes. Hence animals might not expect such changes and, not realizing them, fail to respond to them. The third reason may be a habit of animals not to consult their magnetic compass all the time. Self-produced motion would change the input of the magnetoreceptors, and to avoid dealing with problems arising from this, animals might normally ignore magnetic directional information, calling upon it only when it is required for orientation and navigation. In this light, it is interesting to consider the few positive cases of magnetic conditioning in birds and mammals. A first successful conditioning with pigeons in the 1970s involved a two-way choice, in which the pigeons had to move though a larger flight tunnel and select a feeding box at the right or left side, with the correct alternative indicated by a higher or lower magnetic intensity [4]. It was recently reproduced using the presence or absence of a magnetic anomaly as stimulus [5]. Another recent study with pigeons used an anomaly as a ‘magnetic landmark’ to indicate hidden food in an open arena [6], and in a study with rats, a magnetic anomaly indicated the correct arm of an eight-arm radial maze [7]. These successful studies had common features: the animals were not confined to a small Skinner box, but had room to move about, and the stimuli consisted of changes in magnetic intensity. Even more striking is the conditioning of animals to magnetic directions, which, for a long time, had seemed impossible. Such conditioning was first obtained in young domestic chickens imprinted on a red table-tennis ball: the chicks were trained to locate the ball behind one of four equal screens in the corners of the square test apparatus, with the magnetic direction indicating the correct screen. When the magnetic north had been shifted, the chicks moved to the corner that was now in the correct magnetic direction [8]. The paper by Voss et al. [9] in this journal is another clear example of the conditioned compass response in birds and uses a similar test paradigm: the zebra finches had to select the feeder in the correct EDITORIAL NEUROREPORT