Further efforts at training pigeons to discriminate changes in the geomagnetic field.

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295
J. exp. Biol. 173, 295–299 (1992)
Printed in Great Britain © The Company of Biologists Limited 1992
*To whom reprint requests should be sent.
Key words: pigeon, magnetic sensitivity, magnetoreception, training, Columba livia.
SHORT COMMUNICATION
FURTHER EFFORTS AT TRAINING PIGEONS TO
DISCRIMINATE CHANGES IN THE GEOMAGNETIC FIELD
BY P. A. COUVILLON, ANNE M. ASAM AND M. E. BITTERMAN*
Békésy Laboratory of Neurobiology, University of Hawaii, 1993 East-West Road,
Honolulu, HI 96822, USA
Accepted 28 July 1992
Although magnetic sensitivity in pigeons can reasonably be inferred from the
impairment of homing by magnetic attachments to their heads (e.g. Keeton, 1971;
Walcott and Green, 1974), which have been found to contain magnetite (Walcott et al.
1979), attempts to develop training methods suitable for systematic psychophysical
analysis have been largely unsuccessful. Of four classical conditioning experiments with
magnetic change as the conditioned stimulus, shock as the unconditioned stimulus and
overt activity (Orgel and Smith, 1954) or cardiac acceleration (Beaugrand, 1976;
Kreithen and Keeton, 1974; Reille, 1968) as the conditioned response, only one (Reille’s)
gave any indication of conditioning. Of three experiments in which pigeons were
rewarded with food or water for pecking a target in response to magnetic change (Alsop,
1987; Meyer and Lambe, 1966; Moore et al. 1987), all gave negative results. Bookman
(1977) had some success with a flight tunnel in which his animals were rewarded for
going to one or the other of two food boxes depending on the prevailing magnetic field,
but the results of similar experiments by subsequent investigators were negative (Carman
et al.1987; McIsaac and Kreithen, 1987).
This further training effort with pigeons was encouraged by the finding in recent work
on magnetoreception in honeybees (Walker and Bitterman, 1989; Walker et al.1990) that
the detection of earth-strength anomalies could be facilitated by prior training with a very
strong anomaly. Except for the early experiment on classical activity conditioning (Orgel
and Smith, 1954), pigeons had always before been trained with earth-strength anomalies,
and it seemed reasonable, therefore, to try again with an intense anomaly, using the
versatile and highly efficient pecking technique.
The anomaly was produced with two coplanar, concentric, double-wrapped coils
constructed for the measurement of honeybee magnetic thresholds. The coils were set not
in a laboratory window as before, but in one wall of a plastic and aluminum pigeon
chamber. The inner coil was wound around a piece of Plexiglas tubing, 2.5cm long and
2.5cm in diameter, that now invited the entrance not of a honeybee seeking sucrose, but
of the beak of a pigeon pecking at an illuminated plastic target directly behind it. A

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current of 1A through the coils produced a sharply focused anomaly of 30 times earth
strength in the area of beak insertion (see Walker and Bitterman, 1989, Fig. 1, p. 490, for
details).
As a check on the adequacy of the training procedure to be used with the magnetic
anomaly, nine experienced pigeons were trained first to discriminate the presence or
absence of an 80-dB, 600-Hz tone from a speaker in the roof of the chamber. Each trial in
10 daily sessions of 40 trials began (after an intertrial interval of 30s) with the onset of a
white light behind the translucent pecking target. On half the trials (S+ trials), the first
peck at the target after an interval of 15s turned off the target light and produced the
reward (4-s access to a tray filled with mixed grain). On the remaining (S?) trials, the first
peck after 15s started a 5-s penalty timer that was reset by each subsequent peck, and the
trial ended (without reward) only after the animal refrained from pecking for 5s. The
measure of performance on each trial was the number of pecks in the first 15s. For four of
the nine animals, each peck on an S+ trial turned on the tone for 1s; that is, the birds had
to peck the target in order to hear the tone, just as in the following magnetic
discrimination problem they would have to peck the target to encounter the strong field in
its immediate vicinity. On S? trials, there was no tone. For the remaining five animals,
the tone was produced by pecking on S? but not on S+ trials.
The asymptotic performance of the animals is shown in Fig. 1A, which is based on the
pooled data of the last four training sessions. The two curves, which are plotted in terms
of the mean rate of response on each of 20 S+ and 20 S? trials, give clear evidence of
discrimination [F(1,7)=19.35, P=0.0032]. Whether the tone was S+ or S? made no
296P. A. COUVILLON, A. M. ASAM AND M. E. BITTERMAN
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25
0
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50
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A
S−
S+
B
ToneMagnetic field
051015 20051015 20
Trials
Fig. 1. Mean rate of responding in successive trials within sessions to the rewarded (S+) and
nonrewarded alternative (S?) in training to detect (A) a 600-Hz tone and (B) a marked
increase in magnetic field intensity.

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difference (F<1). The gradual decline in the rate of responding over trials within sessions
that is evident in the curves is common in training of this kind.
The next step was to introduce the magnetic anomaly along with the tone. The coils
were energized at the start of every tone trial (whether S+ or S?) and remained so for the
duration of the trial. Over the first four sessions, the tone was ‘faded out’, which is to say
that its intensity was reduced in stepwise fashion (a standard procedure for transferring
control of discriminative performance from one set of stimuli to another), and in the next
16 sessions the tone was eliminated altogether. As the intensity of the tone was reduced,
differential performance (difference in rate of responding on trials with tone-plus-
anomaly vs no tone in the ambient geomagnetic field) was reduced, disappearing
altogether in the fourth session at the intensity of 62.5dB. In the next 16 sessions, there
was no indication of differential response in the presence vs the absence of the anomaly
alone. Pooled performance in the last four sessions is plotted in Fig. 1B, which shows that
the animals responded both to S+ and to S? at the same rate as to S+ in the tone vs no
tone discrimination.
On subsequent days, there was refresher training on the tone vs no tone discrimination
until performance like that shown in Fig. 1A was re-established, following which there
was further training on the anomaly vs ambient field discrimination, but now the anomaly
was time-varying in a 1-Hz square wave. (The coils were energized once each second for
a period of 0.5s.) No sign of magnetic discrimination appeared in more than 20 training
sessions, during which the performance of the animals resembled that shown in Fig. 1B.
Despite these negative results, it was tempting to look further for evidence of a learned
response to magnetic change, now in direction rather than intensity. The goal was to
determine whether the birds could detect a simple 90˚ shift in field direction but with
approximately the same intensity. The field direction was shifted by the use of a large pair
of square coils, 122cm to the side and separated by 73cm – a square analog of circular
Helmholtz coils yielding optimal field uniformity (Lee-Whiting, 1957). The coils were so
aligned that when activated they produced a NE-to-SW horizontal magnetic component,
shifting the field from north to west. In addition, the ambient field intensity increased
from 60 to 70?T (Wiltschko, 1972). The small coils at the pecking target were removed
and the entire chamber, with the pigeon facing north, was placed between the large coils.
Again, in this situation the animals were trained in two tasks, one to discriminate the
presence of a continuous tone (presented independently of response) from its absence,
and the other to discriminate change in magnetic field direction (produced by
continuously energizing the square coils) from the ambient direction. For the animals
previously trained with tone as S+, tone continued to be S+, and for the others the tone
was S?; for animals previously trained with the magnetic anomaly as S+, the shift in
direction was S+, and for the others the shift was S?.
A simplified, free-operant training procedure was used. In each 30-min training
session, 3-min S+ and S? presentations were regularly alternated. In S+ segments, pecks
at the target were rewarded with 4s of mixed grain on the average of once per minute (a
VI-1min schedule); in S? segments, there was no reward. Under these conditions, as
before, the animals mastered the tone discrimination but not the magnetic discrimination.
In Fig. 2A, asymptotic performance in the tone problem (pooled over the last four
297
Magnetic conditioning in pigeons

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training sessions) is plotted in terms of mean rate of response to S+ and S? in each
segment. The difference in response to the two stimuli is highly significant
[F(1,7)=20.37, P=0.0028] regardless of whether the tone was S+ or S? (F<1). In the
directional problem, the animals gave no evidence of discrimination, even after 40
sessions. Pooled performance in the last four sessions of training in that problem is
plotted in Fig. 2B.
Here, then, is another report of failure to train confined pigeons to discriminate changes
in the ambient geomagnetic field. To judge from work with honeybees (Walker et al.
1989), these failures may reflect not the absence of magnetoreception in pigeons, but only
our ignorance of the circumstances under which magnetic information is processed by the
animals, which may be such as to make formal learning studies impractical. Although it
would be interesting to try to define those circumstances, the easiest avenue to
understanding the magnetosensory system in itself may be found in physiological
preparations.
This project was supported by Minority Access to Research Careers grant
GMO7684–13 and Research Centers in Minority Institutions grant RR-03061 from the
National Institutes of Health. We thank Joseph L. Kirschvink and Michael M. Walker for
advice on magnetic arrangements and measurements.
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298P. A. COUVILLON, A. M. ASAM AND M. E. BITTERMAN
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A
S+
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Trials
Fig. 2. Mean rate of responding in successive trials within sessions to the rewarded (S+) and
nonrewarded alternative (S?) in training to detect (A) a 600-Hz tone and (B) a 90˚ change in
magnetic field direction.

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