AJP 308

American Journal of Primatology 41:323–329 (1997)

BRIEF REPORT
Auditory Behavioral Thresholds for Japanese Macaques
Using Insert Earphones
DAVID W. SMITH* AND VALERIE B. OLSZYK
Hearing Research Laboratories, Division of Otolaryngology-Head and Neck Surgery,
Duke University Medical Center, Durham, North Carolina

The goal of this study was to measure behavioral auditory thresholds in

four Japanese macaques. Animals were trained using food as a reward
in an operant reinforcement paradigm. Stimuli were 1-s sinusoids with
10-ms rise/fall times delivered through insert earphones (Etymotic ER-
1) having expandable foam eartips. The animals generally produced
threshold contours similar in shape to those reported for other macaques
species, except that the low-frequency thresholds may have been slightly
higher in the present studies. At middle and high frequencies, thresh-
olds fell at the lower extreme of the range previously reported in other
macaque species. The possible difference in low-frequency thresholds
may have been a result of either transducer and calibration differ-
ences between studies or true species variations, or both. Though some-
what limited at high frequencies, the insert earphones used in these
studies offer more reliable calibrations, less susceptibility to changes
in positioning with movement of the animal, and greater interaural
attenuation. Am. J. Primatol. 41:323–329, 1997. © 1997 Wiley-Liss, Inc.

Key words: Japanese macaques (M. fuscata); behavioral auditory

thresholds; insert earphones; animal psychophysics

INTRODUCTION
Because of its pleasant behavioral disposition and unique vocal repertoire,
the Japanese macaque (Macaca fuscata) has served as subject in numerous pre-
vious studies of auditory behavior. A partial list includes studies of the voicing
and place features of speech perception [Kuhl & Padden, 1982, 1983]; discrimi-
nation of speech format frequency [Sommers et al., 1992]; perception of commu-
nication sounds [May et al., 1989]; and effects of cortical lesions on detection
threshold [Heffner & Heffner, 1986, 1989]. Somewhat surprisingly, then, we can
find no normative auditory threshold contours for the species in the literature.
These threshold data also provide a necessary framework for interpreting the
acoustic perceptual abilities of the Japanese macaque.

*Correspondence to: Dr. David W. Smith, Director, Hearing Research Laboratories, Division of Oto-
laryngology-Head and Neck Surgery, Box 3550, Duke University Medical Center, Durham, NC 27710.

Received for publication 8 July 1996; revision accepted 11 November 1996

© 1997 Wiley-Liss, Inc.

324 / Smith and Olszyk

In any behavioral study of absolute auditory thresholds, it is important that

factors influencing data variability be controlled as much as possible. Two of the
control methods commonly employed are use of sound-attenuating chambers and
careful calibration of transducers. The latter, however, always includes variabili-
ties in head size and headphone fit across subjects, which alters the frequency
response of the earphone. Also, for a single animal, daily differences in head-
phone placement and animal movement during the test session are additional,
considerable sources of error.
Potential sources of error can be reduced by using commercial insertable
earphones. The earphone foam tips, inserted into the ear canal of the animal,
expand to fill the canal, allowing more repeatable day-to-day placement. When
adequately inserted, the foam eartip holds the earphone in place and, since the
sound is transmitted from the actual transducer box through 25 cm of flexible
tubing, its placement in the canal is not affected by the movement of the animal’s
head. Only one study that we could identify adopted such a strategy. Heffner and
Heffner [1989] used headphones attached to earmolds via plastic tubing to mea-
sure changes in auditory thresholds for Japanese macaques (plotted relative to
an average of thresholds for other macaque species) following cortical lesions.
The investigators reported that the insert earphone arrangement permitted the
animals to move in their restraint chairs while minimizing disruption in the
placement of the transducer.
An important additional benefit of the form-fitted foam eartip is a substan-
tial increase in intra-aural attenuation over more typical earphones fitted with
supraaural and circumaural-type cushions. In our laboratory, we have measured
this increase in attenuation as an additional 20–30 dB at frequencies over the
macaque auditory range.
In the present studies, we sought to determine absolute auditory thresholds
in Japanese macaques and to exploit the advantages of insert earphones for psy-
chophysical testing of nonhuman primates. Using commercial insertable ear-
phones, we measured behavioral thresholds for 1-s sinusoidal stimuli presented
to four juvenile macaques.

METHODS
Subjects
Four juvenile male Japanese macaques (M. fuscata) with no history of otitis
media served as subjects in this study. All weighed between 5 and 9 kg at the
outset of the study and were maintained on a calorie-restricted diet to facilitate
the use of food as a reward in an operant reinforcement paradigm for training
and testing.
The care and use of the animals in this research was approved by the Duke
University Institutional Animal Care and Use Committee.

Behavioral Apparatus
All behavioral test sessions were carried out in two individual-sized, single-
walled wound-attenuating chambers (Acoustic Systems, Austin, TX), that were
housed inside a large, double-walled sound-attenuating chamber (Industrial Acous-
tics Company, Brooklyn, NY). A custom-designed restraint chair was affixed to
each test chamber to restrict movement of the animals relative to the testing
apparatus. Head movement was restricted by placing the animal’s muzzle through
a set of uprights and a stop behind the head. A feeder trough was mounted to the
 Auditory Thresholds for Japanese Macaques / 325

chair within easy reach of the animal’s mouth. The wall directly in front of the
animal contained a mounted response key and a cue light that served to commu-
nicate the experimental conditions to the animal at all times. Stimulus presenta-
tion and all experimental parameters were computer controlled.

Stimuli, Transducers, and Calibration

All stimuli were pure tones generated digitally by a PC-based waveform gen-
erator and a digital-to-analog converter (Tucker-Davis Technologies, Gainesville,
FL). The output of the digital-to-analog convertor was passed successively through
two programmable attenuators (Tucker-Davis Technologies), an anti-aliasing fil-
ter, and a passive attenuator to reduce line noise, to Etymotic ER-1 insert ear-
phones (Etymotic Research, Elk Grove Village, IL). The earphone boxes were
connected to the head stop so that, when the earphone tip was inserted, the tube
of the earphone was out of the reach of the animal. The earphone terminated in
a 10-mm-long pediatric foam eartip, which was compressed and inserted to a
depth of approximately 5 mm. Once inserted, the eartip expanded to a tight fit
that was sufficient to hold the earphone in place without moving during the test
sessions.
A separate calibration was performed in an artificial ear canal for each in-
sert earphone. The dimensions of the artificial canal were determined by dissect-
ing and taking diameter and length measurements in a M. fuscata cadaver head.
In order to determine the length of the ear canal from the eartip to the tympanic
membrane, a foam eartip was inserted into the cadaver ear to a depth compa-
rable to that used in behavioral testing. The tympanic membrane end of the
artificial canal was fitted with a 1/4 inch B & K (Type 4136; Brüel & Kjær,
Marlborough, MA) condenser microphone. A periodic, pseudorandom electrical
noise was presented to the headphone with a clock rate of 200 kHz and a period
of 20.48 ms. The microphone signal was amplified by a B & K 2610 measuring
amplifier and sampled by a PC-based, 16-bit analog-to-digital convertor. Both
the microphone signal and digital-to-analog output were averaged by the collec-
tion computer over 200 cycles of pseudorandom noise. The spectra of the aver-
aged signals were computed by Fourier Transform, and were corrected according
to the frequency/phase response of the probe microphone, to compute the actual
acoustic spectrum. Finally, the system transfer function was computed as a ratio
of the two spectra.
Pure-tone thresholds were measured for 1-s sinusoidal stimuli at frequencies
between 73 Hz and 30.5 kHz. The exact frequencies tested in each animal were
dependent on the precise location of variations found in the frequency response
measured in each earphone. In general, the frequency response was relatively
flat (± 15 dB) between 50 Hz and 16.0 kHz, then decreased rapidly to approxi-
mately 20.0 kHz. In all earphones tested, a pronounced peak occurred in the
spectrum between approximately 25.0 and 35.0 kHz. In this range sound pres-
sure levels were comparable to those measured at lower frequencies and were
sufficient to permit threshold testing in our animals.

Behavioral Procedure
The behavioral procedures used in this study were comparable to those used
and described in detail previously [Moody et al., 1975; Smith et al., 1987]. Briefly,
we trained the animals by applying positive reinforcement in an operant rein-
forcement paradigm. We presented the subjects with a flashing cue light and
326 / Smith and Olszyk

trained them to initiate a trial by making contact with the response lever. When
contact was made, the light would remain on, without flashing, for the duration
of the trial sequence. If the subject maintained contact with the lever through
the required hold intervals (1–8 s, with an average delay of 5 s), the test stimu-
lus was presented and the animal was required to release the key to indicate
signal detection. A correct response (i.e., releasing the key within 0.8 s of the
onset of the signal) was followed by delivery of a 190-mg banana-flavored pellet
(P.J. Noyes, Lancaster, NH) through the feeder trough. Release of the lever at
any other time (i.e., a false alarm) resulted in a 5-s timeout, during which the
cue light was extinguished and the subject was unable to initiate a subsequent
trial sequence. Both ears were fitted with earphones and tested each day. The
right-left order of testing was randomized on a daily basis.
Stimulus intensity at the outset of a trial sequence was set at approximately
35 dB above the typical threshold for that frequency. Thresholds were deter-
mined using a tracking procedure, where stimulus intensity was adjusted on a
trial-to-trial basis by decreasing the intensity 5-dB for the subsequent trial fol-
lowing a correct response. Likewise, a miss resulted in a 5-dB increase in stimu-
lus intensity for the subsequent trial. The change from a hit to a miss, or vice
versa, defined a transition, and eight transitions were presented at each fre-
quency. Threshold for a give frequency was defined as the stimulus intensity at
which 50% signal detection was reported over the last six transitions. Following
determination of threshold for a given frequency, the stimulus frequency was
switched by computer and another tone frequency was selected randomly from
the stimulus list.
Twenty percent of all trials were “catch trials,” where all experimental pa-
rameters were identical to a test-tone trial, except the test signal was withheld.
Routinely, in summary data calculations, we do not include data from sessions
where the subject responds to more than 20% of the catch trials. In the present
studies, however, there were no such sessions, and the average response to catch
trial rate was approximately 1%.
Data were collected in daily testing sessions lasting from 2.5 to 3.5 hours.
Thresholds presented here are the average of six thresholds at each frequency.

RESULTS
Figure 1 presents behavioral threshold contours for both right and left ears
of subjects M03, M04, M05, and M06 for 1-s stimuli. The shape of the contours
was similar in both ears and across all subjects. The absolute level of contours,
however, varied somewhat across subjects with subject M05 being most sensitive
and subject M03 the least. The difference between these animals was greatest at
low frequencies (approximately 17 dB at 500 Hz), with thresholds being within 5
dB above 4.0 kHz. We generally found that thresholds did not vary substantially
across animals when frequencies were above 2.0 kHz.

DISCUSSION
Figure 2 compares the average and range of both ears in all subjects of M.
fuscata from the present studies with the range for threshold contours reported
in the literature for several other macaque species. (The studies used compa-
rable operant reinforcement techniques and closed-field transducers.) The bold
line in Figure 2 represents the average of all threshold functions presented in
Figure 1. In agreement with threshold data reported in other macaque species,
 Auditory Thresholds for Japanese Macaques / 327

Fig. 1. Absolute auditory thresholds, measured behaviorally, in both ears of subjects (a) M03, (b) M04, (c)
M05, and (d) M06. Bars = mean ± SD.

the auditory range of M. fuscata extends from below 100 Hz to above 31.0 kHz,
the highest frequency we were able to test given the high-frequency limitations
of the ER-1 transducers. Differences were apparent, however, in the level of the
low-frequency thresholds between M. fuscata and thresholds measured in other
macaque species: The range of M. fuscata thresholds at 710 Hz and below over-
laps the range of thresholds from the literature, with the exception of 250 Hz.
Nevertheless, the averaged threshold curve, across all four subjects and for both
ears, falls consistently above the range of the macaque literature for frequencies
below 1.0 kHz.
At middle and high frequencies, above 2.0 kHz, the threshold ranges from the
literature and the present study show considerable overlap, though at 4.0 kHz and
above the M. fuscata average falls toward the lower limit of the literature range.
The data reported here do not allow resolution of the question of whether
the differences at low frequency are due to either, or both, real species differ-
ences or differences in transducer and calibration technique between studies.
According to Pfingst et al. [1975] the characteristics of the behavioral audiogram
can be significantly influenced by the techniques used in calibrating the trans-
ducers and these differences are greatest at low frequencies. For example, a trans-
ducer calibration made on a 6-cm3 coupler would, when applied to the much
smaller volume monkey external ear, underestimate low-frequency sound pres-
sure levels and, thereby, yield artificially low behavioral thresholds. The present
study employed a calibration procedure that should provide for an accurate esti-
mation of sound pressure levels near the tympanic membrane.
328 / Smith and Olszyk

Fig. 2. Range and average of thresholds for both ears in all Macaca fuscata subjects (horizontal cross-
hatching) plotted with the range of thresholds from the literature for monkeys from the genus Macaca
(vertical cross-hatching) [Stebbins et al., 1966 (M. fascicularis and M. nemestrina); Stebbins, 1973 (M. arc-
toides, M. fasicularis, M. mulatta, and M. nemestrina); Pfingst et al., 1975 (M. mulatta), 1978 (M. mulatta);
Lonsbury-Martin & Martin, 1981 (M. mulatta)].

Our experience with supraaural and circumaural-type headphones, that move-

ment of an animal’s head caused not only physical displacement of the earphone
relative to the ear canal but also occlusion of the tragus and ear canal [see also
Pfingst et al., 1975], persuaded us to test insert earphones, a technique compa-
rable to that employed by Heffner and Heffner [1989]. They reported that the
flexible tubing connecting the transducer to the in-the-canal mold permits move-
ment of the animal’s head without any disruption of the eartip in the canal. In
our study, the eartips never became displaced because of animal movement. More-
over, our previous studies produced considerably more variability of low-frequency
thresholds, as high as 18–20 dB, for measures repeated within a session. The
present thresholds measured with insert earphones produced SDs, in the worst
cases, of less than half the previous amounts.

ACKNOWLEDGMENTS
The authors are indebted to Mr. Karl E.M. Konrad for his assistance in fab-
ricating the test chambers and developing the software facilities to conduct the
described experiments. We also thank Dr. Chris van den Honert for his collabo-
ration concerning the calibration algorithm and sound level measurements. Edi-
torial assistance was provided by Ms. Ann Tamariz. This research was funded by
 Auditory Thresholds for Japanese Macaques / 329
the National Institutes of Health, National Institute for Deafness and Other Com-
munication Disorders (DC 001692).
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