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Conditioned suppression/avoidance as a procedure for testing
hearing in birds: The domestic pigeon (Columba livia)
Henry E. Heffner &Gimseong Koay &Evan M. Hill &
Rickye S. Heffner
Published online: 6 October 2012
#Psychonomic Society, Inc. 2012
Abstract Although the domestic pigeon is commonly used
in learning experiments, it is a notoriously difficult subject
in auditory psychophysical experiments, even those in
which it need only respond when it detects a sound. This
is because pigeons tend to respond in the absence of sound
—that is, they have a high false-positive rate—which makes
it difficult to determine a pigeon’s audiogram. However,
false positives are easily controlled in the method of condi-
tioned suppression/avoidance, in which a pigeon is trained
to peck a key to obtain food and to stop pecking whenever it
detects a sound that signals impending electric shock. Here,
we describe how to determine psychophysical thresholds in
pigeons using a method of conditioned suppression in which
avoidable shock is delivered through a bead chain wrapped
around the base of a pigeon’s wings. The resulting audio-
gram spans the range from 2 to 8000 Hz; it falls approxi-
mately in the middle of the distribution of previous pigeon
audiograms and supports the finding of Kreithen and Quine
(Journal of Comparative Physiology 129:1–4, 1979) that
pigeons hear infrasound.
Keywords Pigeon .Conditioned suppression .Avoidance
conditioning .Psychophysical procedures .Audiogram .
Infrasound
Introduction
The comparative study of avian hearing is of particular
interest because some species appear to be unusually sensi-
tive to low-frequency sound. However, how widespread this
sensitivity might be is not known, as few studies in birds
have examined their low-frequency hearing (cf. Dooling,
Lohr, & Dent, 1985). Although determining the audiogram
of some birds presents no special problems, others are so
difficult to train on auditory tasks that it has been suggested
that a physiological measure, the auditory brainstem re-
sponse, be used instead (Noirot, Brittan-Powell, & Dooling,
2011). However, the auditory brainstem response is not a
good measure of pure-tone behavioral sensitivity, as it
depends on the synchronous firing of neurons evoked by
brief and impure tones (e.g., Elberling & Don, 2007). Thus,
it is important to find a behavioral procedure that works well
with a broad range of species, including those species that
are difficult to test.
Surprisingly, one of the most difficult birds to train on
auditory tasks has been the domestic pigeon. Although
pigeons are widely used in studies of learning, they do not
perform well on tasks in which they are rewarded for mak-
ing a response when a sound is presented, because they have
a high false-positive rate and often respond in the absence of
the sound (e.g., Stebbins, 1970). One approach to reducing
their false-positive rate has been to avoid rewarding a pi-
geon for accidently responding to a subthreshold sound by
only rewarding it for responding to obviously audible
sounds (e.g., Harrison & Furumoto, 1971). However, this
procedure risks training an animal to ignore sounds near
threshold. Another approach has been to punish false pos-
itives with a short wait or error time out (ETO) before an
animal can respond again for food. However the ETOs used
with pigeons have tended to be long, with the result that in
one case, the animals had to be tested in 12-h overnight
sessions (Hienz, Sinnott, & Sachs, 1977).
There is, however, a procedure for testing hearing that
allows for effective control of false positives and other
errors, and that is the method of conditioned suppression.
FirstusedbyDalton(1967), this procedure consists of
H. E. Heffner (*):G. Koay :E. M. Hill :R. S. Heffner
Department of Psychology, University of Toledo,
Toledo, Ohio 43606, USA
e-mail: Henry.Heffner@utoledo.edu
Behav Res (2013) 45:383–392
DOI 10.3758/s13428-012-0269-y
training a pigeon to peck a key to obtain food and to stop
(suppress) its pecking whenever it detects a sound that
signals impending electric shock. False positives, in this
case, are kept low by adjusting the level of the shock and/
or by increasing the rate of the reward. Although condi-
tioned suppression has been used to test hearing in a wide
variety of mammals (e.g., Heffner & Heffner, 1995), it has
never been used on birds by other researchers, perhaps
because the procedure used by Dalton administered the
shock via surgically implanted electrodes, which was done
because birds have no exposed fleshy surfaces on their feet
on which to make reliable electrical contact for foot shock.
Recently, we became interested in the hearing abilities of
birds, especially as they compare with mammals, and began
testing the hearing of pigeons. Although we initially trained
the pigeons to respond when they detected a sound, we soon
found, as had others, that pigeons have a high false-alarm
rate that makes it difficult to obtain reliable thresholds. We
then turned to the method of conditioned suppression using
avoidable shock, and we found that the pigeons could be
easily trained to give reliable thresholds.
This report demonstrates the utility of conditioned sup-
pression in obtaining auditory thresholds in pigeons, and
probably in birds generally. The procedure used here dif-
fers from the procedure used by Dalton (1967) in several
ways. First, the original conditioned suppression procedure
used unavoidable shock, whereas our animals were able to
passively avoid shock by not responding (suppressing)
when a sound was presented, a modification that increases
the number of trials that can be given in a session. Second,
Dalton administered shock through surgically implanted
electrodes wrapped around the pubic bone; we adminis-
tered the shock noninvasively, through bead chains
wrapped around the base of each wing (Hoffman, 1960;
Honig & Slivka, 1964). Third, Dalton required pigeons to
stop pecking for 20 s; we required pigeons to stop pecking
for only 0.3 s, a change that reduced the response cost to
the animal, since it could not earn a reward during that
time. Finally, we used a different suppression ratio to
calculate an animal’s performance, one that reduced the
raw hit rate by the proportion attributable to false alarms
(Heffner & Heffner, 1995).
Method
We used the method of conditioned suppression/avoidance
to obtain absolute thresholds on pigeons for pure tones
ranging from 2 to 8000 Hz. This consisted of training the
birds to peck a key to obtain access to food and to stop
pecking when a tone was turned on, in order to avoid
electric shock that was delivered through bead chains that
the pigeons wore at the base of their wings.
The present procedure is a modification of the original
conditioned suppression procedure that we began using
many years ago (e.g., Heffner & Masterton, 1970); the
change to avoidable shock was one of several modifications
that we have made. However, using avoidable shock
changes the procedure from classical “conditioned suppres-
sion”to an “avoidance”or “discriminated punishment”pro-
cedure (e.g., Church, Wooten, & Matthews, 1970; Goodall,
1984). Nevertheless, we have retained “conditioned sup-
pression”in the name while noting that the shock is avoid-
able, because it distinguishes this procedure from other
animal psychophysical procedures, all of which require an
animal to make a response when it detects a sound (cf.
Klump, Dooling, Fay, & Stebbins, 1995). This is a crucial
difference: Because ceasing activity or freezing is the natu-
ral response of many animals when a stimulus that signals
danger is detected, the use of suppression to indicate that an
animal has detected a sound simplifies training and accel-
erates testing. Thus, whereas from a learning standpoint
there are important differences between conditioned sup-
pression and discriminated punishment, from the standpoint
of animal psychophysical testing, the differences are small,
though not unimportant (e.g., there is evidence that using
avoidable shock enhances suppression; see Church et al.,
1970; Goodall, 1984).
Subjects
Five homing pigeons (Columba livia), obtained from a local
breeder, were used in this study. The animals were between
3 and 4 years old at the beginning of testing and were
housed in cages with access to grit and water. Pigeon food
(a grain mixture) was used as a reward, and the animals were
weighed daily during testing to ensure that they maintained
a healthy body weight. After completion of the audiogram,
the eardrums of two of the pigeons were ruptured and the
animals were retested, to demonstrate that they were using
their ears to detect the low-frequency tones. The use of
animals in this study was approved by the University of
Toledo Animal Care and Use Committee.
Behavioral apparatus
Testing was conducted in a double-walled sound chamber
(IAC Model 1204; Industrial Acoustics Co., Bronx, NY;
2.55 × 2.75 × 2.05 m), the walls and ceiling of which were
lined with egg-crate foam, and the floor was carpeted to
reduce sound reflections. The equipment used for behavioral
control and stimulus generation was located outside the
chamber, and the pigeons were monitored over a closed-
circuit television. To avoid sound reflections, the pigeons
were tested in a cage (50 × 30 × 42 cm) constructed of half-
inch (0.127-cm) wire mesh, which was mounted 98 cm
384 Behav Res (2013) 45:383–392
above the floor on a tripod. Wire mesh fencing was inserted
inside the cage, narrowing the width to 10 cm, which limited
a pigeon’s movement while allowing it to easily turn around.
Because standard pigeon response keys are large and would
obstruct the sound field, a response key was constructed
using a set of normally open relay contacts with a plastic
disk (15-mm diameter, 4 mm thick) containing a green LED
embedded in it. The response key was mounted vertically
18 cm above the floor of the cage so that the pigeons could
easily peck it to obtain food. The LED embedded in the key
was normally on and provided feedback that the key had
been depressed by turning off momentarily when a pigeon
depressed the key and made contact closure. Access to
pigeon food was provided by a solenoid-operated food tray
that, when operated, would come up underneath the bottom
of the cage in front of the response key so as to allow an
animal to eat from it for 1.65 s; the entire feeder mechanism
was below the level of the cage floor so that it would not
interfere with the sound field.
Finally, electric shock was provided by a shock generator
that was connected via alligator clips hanging from the top
of the cage to the bead chains worn by the pigeons (for a
description of the bead chain procedure for administering
shock to pigeons, see Hoffman, 1960; Stein, Hoffman, &
Stitt, 1971; for its use on small birds, see Hoffman & Ratner,
1974). The animals were trained and tested using shock
levels of 0.14–0.23 ma for a 1-s duration, with the level
adjusted for each animal to the lowest level that produced a
consistent avoidance response to an obviously audible sig-
nal. A 25-W light bulb, placed above and behind the cage,
was turned on whenever the shock was on.
Acoustical procedures
Pure tones were generated (Agilent 33220A function gen-
erator), attenuated (Coulbourn S85-08 programmable atten-
uator), and gated on and off (Coulbourn S84-04 rise-fall
gate) at zero crossing, with a 20-ms rise–decay for signals
above 250 Hz, and 200 ms for lower frequencies. The sine
wave for frequencies above 4 Hz was filtered with a band-
pass filter (Krohn-Hite 3550) set 1/3 octave above and
below the tone’s frequency. Finally, the signal was amplified
(Crown D-75 amplifier for frequencies above 16 Hz and an
Adcom GFA 545 amplifier for lower frequencies), moni-
tored on an oscilloscope, and sent to a loudspeaker: The
loudspeakers used were a Motorola KSN1005A piezoelec-
tric speaker for frequencies 4000 to 8000 Hz, a 6-in. RS
2000 Infinity woofer for 250 to 2000 Hz, a Paradigm Servo
15 subwoofer for 8 to 125 Hz, and a TC Sounds Axis 15-in.
(38.1-cm) subwoofer in an unported enclosure (65 × 65 ×
120 cm) for 2 to 4 Hz and for rechecking thresholds from
8 to 125 Hz. All speakers were placed at least 1 m in front of
the test cage. Testing at frequencies below 250 Hz was
conducted with and without foam pads under the feet of
the tripod on which the test cage was mounted, in order to
investigate the possibility that the animals might be detect-
ing vibrations mediated through the cage floor; thresholds
did not change when the tripod was placed on foam pads.
The sound pressure level (SPL re 20μN/m
2
) of the stim-
ulus was measured and checked for overtones using a 1-in.
(2.54-cm) microphone (Brüel & Kjaer 4145) or a ¼-in.
(0.635-cm) microphone (Brüel & Kjaer 4939, calibrated
down to 2 Hz), a measuring amplifier (Brüel & Kjaer
2610), and a spectrum analyzer (Zonic A&D 3525 FFT
Analyzer). Sound measurements were taken by placing the
microphone in the position occupied by a pigeon’shead
when it was pecking the response key and, for frequencies
of 125 Hz and higher, pointing it directly toward the loud-
speaker (0° incidence). The Paradigm subwoofer, which was
46 × 55 × 51 cm in dimensions, was placed on the floor of
the chamber in front of the test cage; the TC Sounds Axis 15
was placed in front of the cage, turned at 120° so that there
was no chance of a pigeon seeing the movement of the
speaker diaphragm.
Prior training
Before beginning conditioned suppression, two different
procedures were used in an attempt to obtain the pigeons’
audiograms without using electric shock.
The first procedure was a two-choice procedure in which
the pigeons were trained to peck a center response key to
begin a trial and then peck a key to the left if they detected a
tone or a key to the right if no tone was detected; correct
responses were rewarded with food, and incorrect responses
were followed by a short wait or error time out. This pro-
cedure had previously worked with blackbirds and cowbirds
but had been unsuccessful with pigeons (Hienz et al., 1977).
Although we were able to train the pigeons to perform the
two-choice discrimination above chance levels, they were
unable to consistently maintain 90 % correct, a level needed
for threshold testing. Specifically, after 4 months of training,
two pigeons were occasionally able to reach 90 % correct
for groups of 20 trials; one pigeon never scored higher than
85 % correct; and the other two pigeons rarely performed
above chance levels. Therefore, the two-choice procedure
was abandoned.
The second nonshock procedure was a go/no-go proce-
dure that consisted of training the pigeons to peck an “ob-
serving”key to indicate that they were ready to perform the
task, and then to peck a “response”key whenever they
detected a sound; in this task, correct detections were
rewarded with access to food, whereas false positives were
punished with a short wait or error time out (Stebbins,
1970). Although this procedure had been used with pigeons,
it required long error time outs and test sessions lasting 12 h
Behav Res (2013) 45:383–392 385
(Hienz et al., 1977). We were able to obtain apparently
reasonable thresholds with shorter error time outs and ses-
sions of an hour or less, but the thresholds often varied by as
much as 20 dB between individual pigeons, indicating that
the results were probably not valid. Therefore, after 5 months
of training, we abandoned the go/no-go procedure and
turned to the method of conditioned suppression/avoidance
that we have used to test hearing in mammals (Heffner &
Heffner, 1995).
Conditioned suppression/avoidance
The pigeons were trained to peck the response key to obtain
access to food on a variable-ratio schedule of 10 (VR 10).
They were then trained to stop pecking whenever a tone was
presented in order to avoid a mild electric shock. A session
consisted of a series of 2-s trials with a minimum intertrial
interval of 1.5 s, following which the next trial was begun
when the pigeon pecked the key. Because a trial was initi-
ated by a keypeck, the length of the intertrial interval would
exceed 1.5 s if the pigeon stopped to eat a reward or had just
received a shock, but it was typically less than 10 s. The VR
10 was in effect during the entire 2-s trial and the intertrial
interval. The LED in the key was on during both the trial
and the intertrial interval, going off momentarily only when
the pigeon pecked the key; thus, the animals pecked contin-
uously throughout the session, stopping only when they
detected a tone, received a shock, or the food hopper came
up. The response of a pigeon was defined by whether or not
it pecked during the last 300 ms of the trial, giving the
animal sufficient time to react to the signal. Requiring an
animal to suppress pecking for only 300 ms reduced the
response cost to the animal and allowed a lower level of
shock to maintain good performance. If the pigeon did not
peck during this 300-ms period, an avoidance response was
recorded. The avoidance response (withholding keypecks)
was classified as a “hit”if a tone had been presented, and as
a“false alarm”if there had been no tone. Each trial had a
22 % probability of containing a tone.
To reduce the effect of spurious pauses, a trial was not
begun until the pigeon pecked the key, which also meant
that a tone was only presented when an animal’s head was in
position in front of the response key. In addition, rewards
were never given during a 2-s trial, but only during the
intertrial intervals. If a peck during a trial triggered a reward,
the reward was withheld until the first peck in the following
intertrial interval (a peck during the intertrial interval that
triggered a reward did not start a trial); however, if the trial
was a tone trial and the pigeon failed to suppress its pecking,
the reward was not given.
The pigeons, which had previously been trained to peck
the response key for food, were acclimated to pecking with
their bead chains connected to the shock leads for three
sessions (no sound or shock was presented). The initial
suppression training consisted of presenting a salient sound
(broadband noise) followed by shock if a pigeon pecked
during the last 300 ms of the 2-s trials. The performance of
the animals in discriminating noise from silence rose above
chance levels (p< .05, binomial distribution) within 1–3
sessions (average 1.8 sessions) and reached a corrected hit
rate of 95 % or better in 7–11 sessions (average 8.8 ses-
sions). The test sessions typically consisted of 50–100 tone
trials (and associated silent trials) and lasted from 30 to
90 min, depending on the individual pigeon and how much
food it wished to eat.
Hit and false alarm rates were determined for each block
of trials (5–7 tone trials interspersed among 18–25 no-tone
trials) for each frequency. The hit rate was corrected for the
false-alarm rate so as to produce a performance measure
according to the following formula: Performance 0Hit Rate
–(False-Alarm Rate × Hit Rate) (Heffner & Heffner, 1995),
which can also be expressed as Performance 0Hit Rate ×
Correct-Rejection Rate, where Correct-Rejection Rate 01–
False-Alarm Rate. This measure varies from 0 (no hits)to1
(100 % hit rate with no false alarms). Note that this calcu-
lation proportionately reduces the hit rate by the false-alarm
rate observed for each block of trials in each stimulus
condition, rather than by the false-alarm rate averaged for
the session as a whole. This was done because false-alarm
rates varied within a session, depending on the difficulty of
the discrimination.
Absolute thresholds were determined by reducing the
amplitude of a tone in successive blocks of trials until the
pigeon no longer responded to the tone above the .01 chance
level (binomial distribution). Once a preliminary threshold
had been obtained, final threshold determination was con-
ducted by presenting blocks of trials in which the ampli-
tudes of the tones of the different blocks were reduced in 5-
dB steps extending from 10 dB above to 10 dB below the
estimated threshold (the amplitude of the tone within a trial
block did not vary). Trial blocks of higher intensities were
occasionally given to ensure that an animal’s asymptotic
performance had not declined. Threshold was defined as
the amplitude corresponding to a performance of .50, which
was usually determined by interpolation. Threshold testing
for a particular frequency was considered complete when
the thresholds obtained in at least three different sessions
were within 3 dB of each other. After an audiogram had
been completed, each threshold was rechecked to ensure
reliability.
Threshold testing was begun at 1 kHz, with the pigeons
requiring six to eight sessions to reach their lowest threshold
(average, seven sessions). The pigeons reached their lowest
threshold for the next test frequency (2 kHz) in two to four
sessions (average, three sessions), which was typical for the
remaining frequencies. However, by the time that all 15
386 Behav Res (2013) 45:383–392
frequencies had been tested, the animals were experienced
observers, and a threshold could typically be replicated to
within 3 dB in a single session; thus, the results can be
considered accurate to within ±3 dB. Absolute thresholds
for the 15 frequencies, which included obtaining a stable
threshold for each frequency for at least three sessions, were
completed in 85 sessions.
Surgery
To demonstrate that the conditioned suppression/avoidance
procedure is applicable to birds that have been compromised
in some way, two pigeons were anesthetized with isoflorane
(mixed with oxygen), and their eardrums were ruptured with
a double-pronged pick. The animals were then retested to
determine whether they could detect tones from 2 to 63 Hz,
which would also reveal whether the pigeons’sensation of
the low-frequency tones was auditory or vibrotactile in
origin.
Results
The audiograms of the pigeons are shown in Fig. 1; four
animals were tested at 2, 4, 8, 16, 31.5, 63, 125, 250, 500,
1000, 2000, 4000, 5600, and 8000 Hz, with a fifth animal
(pigeon D) being tested at all but 2 and 4 Hz. At a level of
60 dB SPL, the mean audiogram extends from 54 Hz to
6400 Hz, with a best sensitivity of about 14 dB at 1000–
4000 Hz. This is the first pigeon audiogram in which thresh-
olds were obtained for the same individuals for frequencies
ranging from the infrasonic to their high-frequency upper
limit. The close agreement between individual animals sug-
gests that the thresholds are valid.
Pigeons A and E were retested following rupture of their
eardrums, a procedure that would be expected to raise thresh-
olds, especially at low frequencies, but not to entirely abolish
their hearing. To maintain their performance when they could
not hear a tone, blocks of tone trials were alternated with
blocks of trials that contained both the tone and a broadband
noise. The pigeons did not suppress to tones ranging from 2 to
63 Hz at the highest intensities that could be produced, al-
though they did suppress to the broadband noise. This dem-
onstrates that an intact ear is necessary for the pigeon to detect
very low frequencies and that these thresholds are not likely
due to somatosensory responses to vibration. The pigeons’
eardrums healed back after 10 days, at which time their
thresholds returned to preoperative levels.
Discussion
Comparison with previous pigeon audiograms
Figure 2illustrates how the present results compare with all
of the previous pigeon audiograms except for the low-
frequency audiogram of Kreithen and Quine (1979), which
is compared separately. Although there is noticeable varia-
tion between the different studies, the audiograms generally
show that, beginning at the low frequencies, the pigeon’s
sensitivity gradually increases as frequency is increased,
with a region of best sensitivity from 1 to 4 kHz, followed
by a rapid decrease in sensitivity to an upper hearing limit of
about 8 kHz.
Fig. 1 Audiogram of the
pigeon, as determined by
conditioned suppression/
avoidance. The letters indicate
individual pigeons.
Behav Res (2013) 45:383–392 387
There are several of reasons why studies of the same
species may report different thresholds. One is the uniformity
of the sound field in the vicinity of the animal’s head; if an
animal is allowed to move around within the sound field, it
may not be possible to accurately specify the amplitude of the
sound at its ears. In the present study, the sound was only
presented when an animal was positioned directly in front of
the response key, and the sound field in that location did not
vary. Another source of variation is the behavioral procedure,
and indeed, a number of the studies in Fig. 2reported prob-
lems with the pigeons responding in the absence of sound—
false positives (more on this below). The present study had no
problem with false positives. Finally, it is possible that some
pigeons might have different thresholds due either to inbred
genetics or to abnormalities such as ear mites or middle ear
infection. The pigeons in the present study were the result of
random breeding, and their ears were inspected and found to
be free of any signs of mites or infection.
Figure 3illustrates how the present results compare with
the low-frequency audiogram of Kreithen and Quine (1979).
We found that pigeons are indeed sensitive to very low
frequencies. As compared with humans tested under the
same acoustic conditions (Jackson, Heffner, & Heffner,
1999), the pigeons’better low-frequency hearing emerges
for frequencies below 32 Hz. Thus, as first noted by
Kreithen and Quine, pigeons do hear infrasound, defined
anthropocentrically as low-frequency sounds that are inau-
dible to humans at intensities exceeding 60 dB SPL.
It can also be seen in Fig. 3that the thresholds that we
obtained are noticeably less sensitive than those of Kreithen
and Quine (1979), which may be due to differences in the
ways that the two audiograms were conducted. One
difference is the way in whicharesponsewasdefined.
Specifically, Kreithen and Quine used heart rate condition-
ing in which tones were paired with electric shock, with a
positive response defined as an increase in heart rate of 12 or
more beats per minute; any such definition is necessarily
arbitrary, and choosing a different definition of a response
would have yielded a different threshold. There is no way to
precisely equate thresholds obtained with such a response
with those obtained with an operant yes/no response without
comparing them in the same animals. A second difference is
the attenuation step size; the present study attenuated the
sound in 5-dB steps, whereas Kreithen and Quine often used
larger step sizes, which would result in slightly lower thresh-
olds (Quine, 1979). Finally, Kreithen and Quine tested their
animals in a small pressure box, which makes it difficult to
compare their results with those of other animals tested in
much larger sound chambers. The pigeons in the present
study were tested in the same acoustic conditions used for
testing other species, thereby making direct comparisons
possible. In comparing human and pigeon thresholds, a
recheck of the low-frequency thresholds (125 Hz and lower)
of two human observers, conducted at the time that the
pigeons were tested, found the same thresholds shown for
humans in Fig. 3(neither observer was able to hear 2 Hz at
105 dB). However, regardless of the differences between the
present results and those of Kreithen and Quine, both studies
indicate that pigeons have good low-frequency hearing.
Comparison of psychophysical procedures
A recent report on bird hearing stated that some avian
species cannot be easily tested behaviorally, in which
Fig. 2 Comparison of the
present audiogram (line) with
previously published pigeon
audiograms (only the portion of
the present audiogram that falls
within the range of frequencies
tested by the previous studies is
shown). Note that the thresh-
olds of the present study fall
approximately in the middle of
the distribution of previous
thresholds. The numbers indi-
cate previous studies: 1, Trainer
(1947); 2, Heise (1953); 3,
Dalton (1967); 4, Stebbins
(1970); 5, Harrison and
Furumoto (1971); 6, Hienz
et al. (1977); 7, Goerdel-Leich
and Schwartzkopff (1984).
388 Behav Res (2013) 45:383–392
case the auditory brainstem response may be substituted
(Noirot et al., 2011). Although the authors do not say
what species were untestable, a review of the published
pigeon audiograms reveals that most investigators have
found pigeons to be difficult subjects. Therefore, it is
worth reviewing the four procedures used to test pigeon
hearing for insight into any critical differences in the
methods.
Double-grill box avoidance The earliest pigeon audiogram
appeared in an unpublished dissertation, along with the
audiograms of six other species of birds (Trainer, 1947;
Study 1 in Fig. 2). The pigeons were tested in a double-
grill box in which an animal was required to move from one
compartment of the box to the other whenever it heard a
tone, to avoid electric shock delivered through the floor
bars. With regard to the relative difficulty in training, Train-
er reported that “In numerous cases, most commonly with
the pigeons, extended intervals of up to ten minutes [be-
tween trials] were necessary in order to combat extreme
nervousness.”Apparently, the pigeons had the highest ten-
dency of the seven species to respond in the absence of
sound—that is, the highest false-positive rate.
In the double-grill box avoidance procedure, there is no
easy way to reduce false positives, as an animal can suc-
cessfully avoid shock by continuously crossing back and
forth between the two compartments. Although false pos-
itives can be punished with “counter shock”—that is, shock-
ing an animal when it responds in the absence of sound—
our experience is that this is likely to cause an animal’s
performance to deteriorate to the point at which it complete-
ly ceases to respond.
Go/no-go Four pigeon audiograms have been obtained us-
ing go/no-go procedures in which an animal is trained to
peck a key for food in the presence of a tone and to withhold
responding in the tone’s absence. In the first go/no-go au-
diogram, pigeons were required to wait until a tone was
presented and then to peck a key at least ten times during a
tone interval to receive access to food (Heise, 1953; Study 2
in Fig. 2). To reduce the problem of false positives, the
animals were never reinforced when a tone was within
10 dB of threshold, and long silent periods between trials
were sometimes given to extinguish responding in the ab-
sence of a tone. Nevertheless, of the six pigeons that were
used, one was untrainable, and relatively complete audio-
grams could be obtained on only two of the remaining five
animals.
A second study used a go/no-go procedure in which
false positives were also controlled by not rewarding
keypecks to low-intensity tones (Harrison & Furumoto,
1971). In this study, the pigeons were reinforced with
foodforpeckingakeyinthepresenceofaneasily
audible tone on a variable-interval schedule. After two
months of training, thresholds were obtained by insert-
ing lower intensity tones into a session, but never re-
warding keypecks during these tones. The resulting
audiogram obtained some of the lowest thresholds of
anypigeonaudiogram(Study5inFig.2). The pigeons
may have responded to low-intensity tones in the ab-
sence of reinforcement because of the extensive training
that they received before testing was begun. It is also
possible that the low thresholds were the result of using
a curve-fitting procedure rather than the actual data
points to calculate threshold.
Fig. 3 Comparison of the
present audiogram with the
low-frequency pigeon audio-
gram of Kreithen and Quine
(1979) and with the human au-
diogram (Jackson, Heffner, &
Heffner, 1999). Although the
present audiogram does not
show the pigeons to be as sen-
sitive as does that of Kreithen
and Quine, it does confirm their
previous finding that pigeons
have better low-frequency
hearing than humans do.
Humans, on the other hand,
have better sensitivity in their
mid-frequency range and are
able to hear higher frequencies
than pigeons.
Behav Res (2013) 45:383–392 389
The next study attempted to control the false-positive rate
by adding an “observing”response and by punishing false
positives with an ETO (Stebbins, 1970; Study 4 in Fig. 2).
Specifically, pigeons were trained to peck an observing or
“ready”key, in order to turn on a tone, and then to peck a
“response”key whenever the tone was detected. Although it
was hoped that the observing response would give an animal
something to do while waiting for a tone, the animals still
had high false-positive rates. Thus, Stebbins noted that “We
found the pigeon a recalcitrant subject, as others apparently
have, for auditory experimentation.”
The last pigeon audiogram to use the go/no-go proce-
dure is of particular interest because it demonstrated how
the ability of pigeons to perform auditory detection tasks
compares with that of other species (Hienz et al., 1977;
Study6inFig.2). The authors of this study first attemp-
ted to use a two-choice procedure in which a pigeon
pecked a center key to initiate a trial (a “ready”response)
and then pecked a key to its right, if it detected a tone, or
a key to its left, if no tone was detected. Although red-
wing blackbirds and brown-headed cowbirds learned the
task without difficulty, pigeons did not, despite six
months of training. As a result, audiograms had to be
obtained with a go/no-go procedure similar to that used
by Stebbins (1970); however, the animals required such
long ETOs for punishing false positives that they had to
be tested overnight in 12-h sessions.
In analyzing the difficulties that these studies had with
false-positive responses, it may be noted that the response
of pigeons on auditory generalization tasks is affected by
whether the response key is lit or dark (Honig & Urcuioli,
1981; Rudolph & van Houten, 1977). Specifically,
pigeons show a steep generalization gradient to tonal
frequency when the response key is dark, but not when
it is lighted, indicating that a lighted key is a competing
stimulus that can affect a pigeon’s response to auditory
stimuli. Although this could account for the high false-
positive rate found by Harrison and Furumoto (1971), it
would not account for Heise’s(1953) difficulties, as his
response key was an apparently unlit button attached to a
microswitch. Nor can it provide a simple explanation for
the results of Stebbins (1970)andHienzetal.(1977),
whousedanobservingkeyandaresponsekey,bothof
which were lit. Nevertheless, the effect of lighting the
response key on auditory generalization tasks is important
to keep in mind when designing auditory tests for pigeons
and, perhaps, for other birds.
In summary, the problem of false positives in the go/no-
go procedure has been addressed in two ways. One is by
never rewarding an animal for responding to low-intensity
sounds, which eliminates the possibility that it might be
rewarded for responding when it did not detect a tone, but
runs the risk of training the animal to ignore low-intensity
tones. Another way is to punish false positives with ETOs,
although ETOs do not seem to be as aversive to pigeons as
they are to other species. However, the go/no-go procedure
might work satisfactorily with pigeons if the aversive con-
tingencies were increased by punishing false positives with
mild shock.
Heart rate conditioning Two pigeon audiograms have been
obtained using classical conditioning of heart rate, in which
pairing tones with electric shock causes a pigeon’s heart rate
to increase whenever it detects a tone. Because a positive
response is determined by comparing the heart rate during
tone presentation with the heart rate during the silent inter-
val preceding the tone, it is necessary to keep a pigeon’s
heart rate during the silent intervals from becoming erratic.
Accordingly, the level of shock is kept low and the tone
trials are infrequent.
The first audiogram to use heart rate conditioning in the
pigeon was the low-frequency audiogram by Kreithen and
Quine (1979), which paired tones with shock and defined a
response as an increase in heart rate of 12 or more beats per
minute. To maintain the response, it was necessary to space
trials at least 4 min apart and to limit the number of trials
that could be given in a session. Although, as noted by
Quine (1979), the heart rate response has the advantage of
requiring little training, 85 sessions were needed to obtain
thresholds for 11 frequencies—this is about the same length
of time it took to obtain thresholds for 15 frequencies using
conditioned suppression/avoidance.
The authors of the second study that used heart rate
conditioning to test pigeon hearing also commented on the
need to keep the electric shock “as weak as possible”to
avoid disrupting an animal’s behavior (Goerdel-Leich &
Schwartzkopff, 1984). Although they did not give details
about the procedure, the article they cited for their methods
described a 5-min pause between shock trials, fewer than 20
shock trials per session, and testing every other day, appar-
ently to prevent the shock from disrupting the pigeons’
performances (Shen, 1983). Even these precautions were
not always sufficient, as another study found that three of
11 pigeons had to be excluded from a sound localization
study either because they could not be conditioned or be-
cause they had an irregular heart beat (Lewald, 1989). As
can be seen in Fig. 2(Study 7), the audiogram obtained with
this procedure gives some of the lowest thresholds, although
this may be because threshold was defined as the lowest
intensity that caused an increase in heart rate over baseline
(p< .025) rather than as the 50 % detection level used by the
other studies.
In summary, false positives in heart rate conditioning are
controlled by keeping the level of shock low and allowing
sufficient time between shock trials, although some animals
may still not be testable with this method.
390 Behav Res (2013) 45:383–392
Conditioned suppression/avoidance Prior to the present
study, Dalton (1967) demonstrated the applicability of
conditioned suppression/avoidance for testing hearing in
pigeons by obtaining thresholds for three frequencies
(Study 3 in Fig. 2). Dalton noted that pigeons easily
learned to suppress keypecking for food when a supra-
threshold tone was turned on, showing evidence of
learning in the first 2 days of training. False positives
in conditioned suppression/avoidance—that is, ceasing
to respond in the absence of sound—are controlled
two ways. The first is to reduce the level of the shock
—which, if too high, will cause a pigeon to stop peck-
ing. The second is to increase the frequency of reward
delivery by, for example, changing the variable-ratio
schedule from VR 10 to VR 5. Thus, as has been
noted, conditioned suppression has “the advantages of
aversive control [which controls an animal’s propensity
to suppress] while the ongoing behavior of the animal
[pecking the key] is being maintained on a positive
reinforcement schedule”(Smith, 1970; see also Heffner
& Heffner, 1995).
In summary, conditioned suppression and conditioned
suppression/avoidance have the advantage of allowing fine
control over both misses and false alarms by adjusting both
the reward and shock levels. The validity of the thresholds
obtained is attested by the agreement of thresholds obtained
in different laboratories at different times (e.g., Heffner,
Heffner, Contos, & Ott, 1994). Indeed, as can be seen in
Fig. 2, the average thresholds found by the present study are
within 3 dB of the three thresholds obtained by Dalton
(1967). Given the ability of conditioned suppression/avoid-
ance to easily provide reliable auditory thresholds for even
difficult-to-test birds like pigeons, we see no reason to use
physiological estimates of hearing in birds, because such
measures do not accurately reflect an animal’s behavioral
capacities.
Author note We thank K. Marchetto for conducting the behavioral
tests.
References
Church, R. M., Wooten, C. L., & Matthews, T. J. (1970). Discrimina-
tive punishment and the conditioned emotional response. Learn-
ing and Motivation, 1,1–17.
Dalton, L. W. (1967). Conditioned suppression as a technique for
determination of auditory sensitivity in pigeons. The Journal of
Auditory Research, 7,25–29.
Dooling, R. J., Lohr, B., & Dent, M. L. (1985). Hearing in birds and
reptiles. In R. J. Dooling, R. R. Fay, & A. N. Popper (Eds.),
Comparative hearing: Birds and reptiles (pp. 308–359). New
York, NY: Springer.
Elberling, C., & Don, M. (2007). Detecting and assessing synchronous
neural activity in the temporal domain (SNR, response detection).
In R. F. Burkard, J. J. Eggermont, & M. Don (Eds.), Auditory
evoked potentials (pp. 102–123). Baltimore, MD: Lippincott Wil-
liams & Wilkins.
Goerdel-Leich, A., & Schwartzkopff, J. (1984). The auditory threshold
of the pigeon (Columba livia) by heart-rate conditioning. Natur-
wissenschaften, 71,98–99.
Goodall, G. (1984). Learning due to the response-shock contingency in
signaled punishment. Quarterly Journal of Experimental Psychol-
ogy, 36B, 259–279.
Harrison, J. B., & Furumoto, L. (1971). Pigeon audiograms:
Comparison of evoked potential and behavioral thresholds
in individual birds. The Journal of Auditory Research, 11,
33–42.
Heffner, H. E., & Heffner, R. S. (1995). Conditioned avoidance. In G.
M. Klump, R. J. Dooling, R. R. Fay, & W. C. Stebbins (Eds.),
Methods in comparative psychoacoustics (pp. 49–93). Basel,
Switzerland: Birkhäuser.
Heffner, H. E., Heffner, R. S., Contos, C., & Ott, T. (1994). Audiogram
of the hooded Norway rat. Hearing Research, 73, 244–247.
Heffner, H., & Masterton, B. (1970). Hearing in primitive primates:
Slow Loris (Nycticebus coucang) and Potto (Perodictius potto).
Journal of Comparative and Physiological Psychology, 71, 175–
182.
Heise, G. A. (1953). Auditory thresholds in the pigeon. The American
Journal of Psychology, 66,1–19.
Hienz, R. D., Sinnott, J. M., & Sachs, M. B. (1977). Auditory sensi-
tivity of the redwing blackbird (Agelaius phoeniceus) and brown-
headed cowbird (Molothrus ater). Journal of Comparative and
Physiological Psychology, 91, 1365–1376.
Hoffman, H. S. (1960). A flexible connector for delivering shock to
pigeons. Journal of the Experimental Analysis of Behavior, 3,330.
Hoffman, H. S., & Ratner, A. M. (1974). A shock-delivery system for
newly hatched precocial birds. Journal of the Experimental Anal-
ysis of Behavior, 22, 575–576.
Honig, W. K., & Slivka, R. M. (1964). Stimulus generalization of the
effects of punishment. Journal of the Experimental Analysis of
Behavior, 7,21–25.
Honig, W. K., & Urcuioli, P. J. (1981). The legacy of Guttman
and Kalish (1956): 25 years of research on stimulus gener-
alization. Journal of the Experimental Analysis of Behavior,
36,405–445.
Jackson,L.L.,Heffner,R.S.,&Heffner,H.E.(1999).Free-
field audiogram of the Japanese macaque (Macaca fuscata).
Journal of the Acoustical Society of America, 106,3017–
3023.
Klump, G. M., Dooling, R. J., Fay, R. R., & Stebbins, W. C. (Eds.).
(1995). Methods in comparative psychoacoustics. Basel, Switzer-
land: Birkhäuser.
Kreithen, M. L., & Quine, D. B. (1979). Infrasound detection by the
homing pigeon: A behavioral audiogram. Journal of Comparative
Physiology, 129,1–4.
Lewald, J. (1989). Verhaltensphysiologische und neurophysiologische
Untersuchungen zum Richtungshören der Taube (Columba livia).
Herne, Germany: Verlag für Wissenschaft & Kunst.
Noirot, I. C., Brittan-Powell, E. F., & Dooling, R. J. (2011). Masked
auditory thresholds in three species of birds, as measured by the
auditory brainstem response (L). Journal of the Acoustical Society
of America, 129, 3445–3448.
Quine, D. B. (1979). Infrasound detection and frequency discrimina-
tion by the homing pigeon (Unpublished doctoral dissertation).
Ithaca, NY: Cornell University.
Rudolph, R. L., & van Houten, R. (1977). Auditory stimulus control in
pigeons: Jenkins and Harrison (1960) revisited. Journal of the
Experimental Analysis of Behavior, 27, 327–330.
Behav Res (2013) 45:383–392 391
Shen, J.-X. (1983). A behavioral study of vibrational sensitivity in the pigeon
(Columba livia). Journal of Comparative Physiology, 152,251–255.
Smith, J. (1970). Conditioned suppression as an animal psychophysical
technique. In W. C. Stebbins (Ed.), Animal psychophysics: The
design and conduct of sensory experiments (pp. 125–159). New
York, NY: Appleton-Century-Crofts.
Stebbins, W. (1970). Studies of hearing and hearing loss in the mon-
key. In W. C. Stebbins (Ed.), Animal psychophysics: The design
and conduct of sensory experiments (pp. 41–66). New York, NY:
Appleton-Century-Crofts.
Stein, N., Hoffman, H. S., & Stitt, C. (1971). Collateral behavior of the
pigeon during conditioned suppression of key pecking. Journal of
the Experimental Analysis of Behavior, 15,83–93.
Trainer, J. E. (1947). The auditory acuity of certain birds. In G. S.
Cunningham (Ed.), Abstracts of theses 1946 (pp. 246–251).
Ithaca, NY: Cornell University.
392 Behav Res (2013) 45:383–392
