pure-tone auditory behavioral thresholds in three species of lemurs

Received 26 February 1970 4.6

Pure-Tone Auditory Behavioral Thresholds in Three Species o f Lemurs

CUI•T MITCHELL, RICHARD GILLETTE, •ACK VERNON, AND PAUL HERNAN

Kresge Hearing Research Laboratory, University of Oregon Medical School, Portland, Oregon 97201, and Oregon Regional Primate Center, Beaverton, Oregon 97005

Absolute thresholds were determined for pure tones of frequencies 100 Hz-40 kHz by the method of constant stimuli using a two-bar operant technique. Lemurs of three subspecies were trained to press a white bar to turn on a tone lasting 5 sec. During the tone, a single press on a second (black) bar resulted in food reward. Failure to respond simply terminated the trial. Response in the absence of tone was scored as a false positive response and resulted in a «-sec shock of from 0.6 to 1.3 mA. Thresholds, based on a response probability of 0.5, indicate a lesser sensitivity in the low and middle frequencies than found in the anthropoid primates, but an apparent extension of sensitivity into the higher frequencies beyond the upper-frequency cutoff points found for the anthropoids.

INTRODUCTION

The auditory sensitivity of the anthropoid primates has received a considerable amount of attention in the

literature, both from students of comparative audition and those interested in the utilization of these sub-

human primates as subjects in studies concerned with either experimental acoustics or auditory fatigue. Behavioral and/or electrophysiological estimates of sensitivity have been reported for the chimpanzee (Elder, 1935), the baboon (Wendt, 1934), green mangabey, and squirrel monkeys (Wever et al., 1958; Wendt, 1934; Peterson et al., 1968), four species of macaque monkeys (Clack and Herman, 1963; Behar et al., 1965; Fujita and Elliott, 1965; Stebbins et al., 1966), and the marmoset (Seiden, 1958). In contrast, only recently are data becoming available with refer- ence to the auditory sensitivity of the prosimian sub- order, whose members include such animals as the tree shrew (Peterson et al., 1968; Heffner et al., 1969a), galago (Heffner et al., 1969b), lemur, tarsier, and the loris and the porto (Heffner and Masterton, 1970). Vernon (1967) has recently summarized the literature on both prosimian and anthropoid families and has commented on the paucity of information available for the former group. The present study attempted to enlarge this body of information by investigating the auditory sensitivity of several species of lemur. We chose this representative for several reasons' (a) lemurs,

being geographically isolated on the island of Mada- gascar, remain anatomically similar to fossilized forms of some 50 million years ago; (b) no behavioral data were available for this animal; and (c) the Oregon Regional Primate Center maintains the largest captive population of lemurs in the world.

I. PROCEDURE

A. Subjects

Six lemurs, males and females of each of three species (lemur catta, lemur macaco fulvus, and lemur macaco macaco), served as subjects. Their weights, breeding behavior, and dentition indicate that three were adult and three adolescent (see Table I). All were healthy; one (No. 2023) was extremely fat and had also been previously treated with antibiotics for a jaw infection. The animals were deprived of food and received ad lib water during training and testing. The extent of deprivation may be estimated from the weight data included in Table I.

B. Apparatus

The animals were trained and tested in a small

cage inside a double-walled IAC chamber. Standard audiometric and programming equipment was used to generate and control the sound stimulus, food, and, later, shock. A Western Electric 555 speaker produced

The Journal of the Acoustical Society of America 531

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MITCHELL ET AL.

TABLW. I. Subject identification summary.

Species

Number Sex

Age at end of testing Weight (g) before test Weight during test Percent deprivation

(approx) Weight after test

CATTA FULVUS MACACO

3183 2023 3368 F M F

2 yr 4mo ? 2 yr 1350 3200 1580

1400-1480 2150-2450 1100-1200 ß -- 73 73

1730 2660 1560

3442 2548 2549 M F M

2 yr ? ? 1220 1940 2160

1020-1100 1550-1650 1580-1650 87 82 75

1560 1880 2115

the sound into an open field. The entire chamber was lined with convoluted foam rubber to reduce sound variability. Calibration of the sound field was accomplished with a Briiel & Kj•er -}-in. calibrated microphone, cathode follower, and Sierra model 30lB wave analyzer. A life-size papier-mach• model of a lemur was used during calibration to approximate sound perturbations in the field encountered with the behaving animal. The microphone was mounted over the ear of the model, and the model was moved to six different positions in the field to sample the area favored by the animals during threshold measurements. Table II presents variability in the sound field at each frequency sampled on two separate calibration days; each value then represents the range of 12 separate observations.

C. Training Procedures

The animals were first adapted to handling and transferal procedures until urination and defection moderated and shrieking behavior ceased. These animals are very "skittish" as well as being rare and expensive, and for these reasons, extra care was always taken in handling. Also, for these reasons, the use of shock as a reinforcer was initially rejected. The training procedure itself was modeled after a two-bar method similar to that used by Gourevitch and Hack (1966) and also by Stebbins (1966). The animals were placed

TABLE II. Variability in the sound field. Each observation represents the total range, in decibels of 12 separate estimates of the sound field. See text.

Frequency Variability in dB

100 Hz 6 200 Hz 4 500 Hz 4

1 kHz 6 2 kHz 10 4 kHz 4 8 kHz 8

15 kHz 8 25 kHz 16 40 kHz 19

in a training cage inside the IAC chamber and magazine trained by conventional shaping procedures with pieces of raisins, banana, grape, and pineapple. When they reliably and rapidly ate food, a single black bar was introduced, and bar pressing was shaped. When responses on the black bar for food were both deliberate and frequent, a tone was introduced. From this point on, responses in the presence of tone (R, v) resulted in food reinforcement, and responses in the absence of tone (R?) resulted in a 10-sec, lights-out period. Initially the o• and o• periods were long, and then were progressively shortened to 10 sec. This training continued until the criterion of one R? response per 2 min of s a was reached. This required about 1600 trials or 40 h of training.

When the above criterion was reached, a second bar, white, was introduced and placed about 7 in. from the black bar. A single press on the white bar turned on the tone for 10 sec. Responses on the black bar, while the tone was on, were considered correct "hits" and delivered a pellet of food. Responses on the black bar, when the tone was off, designated as "false positives," resulted in a 10-sec, lights-off period during which both bars were deactivated.

The number of presses on the white bar necessary to turn the tone on was gradually increased via variable ratio schedules to 3, 5, 7, and finally 10 presses. This was done to minimize both alternating behavior and temporal responding. To maintain consistent responding: deprivation on a body weight basis (of about 80%) was begun (see Table I). Animals were then trained to a criterion level of 90% hits and less than 10% false positives. The time-out procedure for the minimization and control of false positives did not prove effective, especially when the intensity of the tone was reduced in the early threshold testing stages. It is easy to see that the control of this behavior is essential to the

interpretation of data, since a high false positive rate vitiates the confidence one may place in any threshold' responding. We therefore introduced a 0.5-sec shock (0.6-1.6 mA) along with the lights out procedure for the control of false positive responses. Although it did bring the false positive rate under control (i.e., down to criterion level or less), it also tended to increase the miss rate, and an empirical balance between food

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AUDITORY THRESHOLDS IN LEMURS

FiG. 1. Auditory thresholds of six lemurs.

80

60

40

20

-20 -

0.

e--e 2025 ß ß 3183

o---o 2548 . ......... . 3442

f a---/• 2549 o ......... o 3368 _

- ............. ".. .............. ." - "ø ...... ?•--,,-•,, .... .. ,' ..'"/ ,'•-,,.'*./" •i'.:•.' "

'•õ.. •'-x. •( ." / -•<. ' ". ß ,:. :•-- '__.,.•_--• ........ .-: ....... õ. - - • ß _ .:...,•,x,•.•: , _ ..... ,_•, ":-'..•. _

0.2 0.5 I 2 4 8 15 25 40

FREQUENCY (kHz)

deprivation and shock had to be carefully maintained. When the 90070 hit-10% false positive criterion was again reached, threshold testing began.

I). Threshold Testing

The threshold was defined as the intensity at which the probability of a response to a tone presentation was 50070. Rough estimations of this point were first assessed by decreasing intensity in five steps of 10 dB each and recording the probability of a response from at least 10 presentations of each intensity. These data were not utilized in the final estimation of threshold.

Starting points for threshold estimates were then placed at about 15 dB above the estimated threshold, based on the previously obtained information. This interval of uncertainty was then explored with steps of 2, 3, or 5 dB, according to the animals performance. For the first three animals (Nos. 2458, 2549, and 2023), data were collected for the middle and lower frequencies first, and followed by the higher frequencies. Order of collection of data was randomized for the other

three subjects. Threshold determination is accomplished by record-

ing the number of correct, incorrect, and false positive responses to stimuli of varying intensities presented in a random fashion. A single "run" consists of 50 such stimuli, 10 trials at each of five intensities. A run was considered acceptable only if it met the following criteria' (a) no more than five false positive responses per block of 50 trials, and (b) no reversals in the data; i.e., an animal may not have a greater number of correct responses to a weaker tone than to a more intense tone. Presentation in a random fashion mini- mizes both over- and under-estimation associated with

ascending and descending series of stimuli. Over the days, different ranges of intensities were presented in order that an eventual series consisted of a number of

performance scores at each of many intensities for

each frequency. Data were considered complete when thresholds on three days were within 6 dB of each other and showed no further reduction in intensity. This criterion worked well for the first-three animals, but the latter three did show fluctuations, which led to a considerably greater number of trials necessary for criterion. In all cases, data over days were com- bined into one plot (percent correct versus intensity) for threshold calculations, and the final estimate was based on a line of best fit derived from these data. In

no case was the estimated crossing 'of the 500-/0 level ever more than 3 dB different from the raw data.

II. RESULTS AND DISCUSSION

Figure 1 presents auditory thresholds obtained in this study from the sample of six lemurs. Several aspects of these data are immediately apparent. First, animal No. 2023 indicates somewhat discrepant thresholds at both 15 and 25 kHz, and no response at all at 40 kHz. Consideration of Primate Center records reveals

two possible reasons for this apparent loss. Although his age is not known, at acquisition in late 1965, he was judged to be an old animal on the basis of weight and dentition. High tone loss with advancing age is not an uncommon phenomenon, and we may be viewing its occurrence in this animal. Further, shortly after acquisition, this animal developed an infection on the left side of the face. Although it responded readily to the application of non-ototoxic antibiotics, this infection may have caused some damage to the auditory system.

As can be seen, with the exception of (a) animal No. 2023 at the higher frequencies and (b) all animals at 4 kHz, over-all agreement is fairly good among animals. Three of the animals, Nos. 2023, 2548, and 3442, did not respond to a 40-kHz stimulus when presented at 55 dB SPL, which was the maximum



18:06:32

MITCHELL ET AL.

ß ß Lemur ß ß Galago a .... a Loris o .......... o Chimpanzee

80 /', .... /', Potto ß .......... ß Marmoset

60 • ß .' ,?' /

. ..... ,,; /

ß I I i I / T: ....,:_%,-.. , _ 20 k- ". '- '-B ..... 1•-<--< -- .--. .: ./ /

I 'ß ...... x x x •, ' '" 'FI. / / / I I / I- '... -,,, ..... ,, .....

'ß .... ß . .. - -. ß ...... // o - ß .... o ...:,,•___•, ß

ß

..... .. - 0 ......... 0" '"...

0 -20 -

0.1 0.2 0.,.5 I 2 4 B

FREQUENCY (kHz)

i I i

15 25 40

Fro. 2. Auditory sensitivity of several selected primates (see text).

intensity our equipment was capable of producing without introducing distortion.

Inspection of the individual records at 4 kHz reveals two separate distributions, separated by about 18 dB. Review of Table I indicates that neither age, sex, nor species accounts for this difference. These data are presented without explanation, and it is interesting to note that other investigators have indicated a "dip" in sensitivity at or near 4 kHz for the chimpanzee (Elder, 1935), the marmoset (Seiden, 1958), and several prosimians (Heffner to be published; Heffner and Masterton, to be published). Figure 2 presents these data, along with the averaged data from the present study (averaging renders the 4-kHz data less apparent). The data from the prosimian forms indicate a lesser over-all sensitivity in the low and middle frequencies than found in the anthropoid primates, but an apparent extension of sensitivity into the higher frequencies beyond the upper frequency cutoff points found for the anthropoids. Stebbins (to be published) most recently has commented on this finding in a review of the literature. The data of the present study support this finding, which is presently being checked in an- other sample of lemurs. Indeed, although at 25 kHz, two of the animals are exhibiting the start of their high-frequency cutoff (see Fig. 2), the remaining four animals demonstrate sensitivity which is within 3 dB or less of their most sensitive threshold. At 40 kHz, two of these animals indicate a threshold which is

within 1 dB of their most sensitive point. Preliminary data from the ongoing extension study indicate thresholds which are slightly more sensitive than indicated in this report.

Finally, we feel constrained to indicate that the two-lever procedure is not to be recommended for further experimental work with the lemur; it is ap-

parently too difficult a task for this animal to learn without long exasperating training and testing sessions. The number of trials necessary to sample a 20-dB range (and meet the established criteria) around the estimated threshold varied from a low of 1680 trials to

a frustratingly high total of 8850 trials; this represents a considerable expenditure of time and effort. More- over, the two-lever procedure appears to work only when shock is used as a deterrent. This was ascertained

in two ways'first, the drastic reduction in the number of false positive responses which occurred with the introduction of shock, and second, a temporary dramatic increase in these responses on a day when, unknown to us, the shock apparatus failed to function. Correction of the equipment malfunction resulted in an immediate decrease in the number of false positive responses. The data gathered on that particular day were not utilized in threshold estimates. The present extension study is a modification of a single-lever shock-avoidance para- digm described by Clack and Herman (1963). Pre- liminary data indicate it is vastly more suitable to the lemur than the previous frustrating technique.

ACKNOWLEDGMENTS

This research was supported by a grant from the National Institute of Neurological Diseases and Stroke, United States Public Health Service. The authors wish

to express their appreciation to Dr. William Montagna, Director of the Oregon Regional Primate Center for his assistance and considerations and to Dr. Bruce

Masterton for making data on the potto, loris, and galago available to us.

* Portions of thb paper were presented to the 78th meeting of the Acoustical Society of America, 4-7 November 1969, in San Diego, California FJ. Acoust. Soc. Amer. 47, 67(A) (1970)].

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AUDITORY THRESHOLDS IN LEMURS

REFERENCES

BEHR, I., CRONHOLM, J. N., and LOEB, M. (1965). "Auditory Sensitivity of the Rhesus Monkey," J. Comp. Physiol. Psychol. 59, 426-433. CLACK, T. D., and HERMAN, P. N. (1963). "A Single-Lever Psychophysical Adjustment Procedure for Measuring Auditory Thresholds in the Monkey," J. Auditory Res. 3, 175-183. ELDER, J. H. (1934). "Auditory Acuity of the Chimpanzee," J. Comp. Psychol. 17, 157-183. FUJtTA, S., and ELLtOTT, D. N. (1965). "Thresholds of Audition for Three Species of Monkey," J. Acoust. Soc. Amer. 37, 139-144. GOUREWTCH, G., and HACK, M. N. (1966). "Audibility in the Rat," J. Comp. Physiol Psychol. 62, 289-294. HEFFNER, H. E., and MASTERTON, B. (1970). "Hearing in Primitive Primates," J. Comp. Physiol. Psychol. (to be published). HErrNER, H., RAWZZA, R., and MASTERSON, B. (1969a). "Hearing in Primitive Mammals. III: Tree Shrew (Tupaia glis)," J. Auditory Res. 9, 12-18. HErrNER, H., R•wzz•, R., and M•S•ERTON, B. (1969b). "Hearing in Primitive Mammals. IV: Bushbaby (Galago senegalensis)," J. Auditory Res. 9, 19-23.

PETERSON, E. A., WRUBLE, S. D., and PONZOLI, V. I. (1968). "Auditory Responses in Tree Shrews and Primates," J. Auditory Res. 8, 345-355. SEIDEN, H. R. (1958). "Auditory Acuity of the Marmoset Monkey (Hapale Ja½½hus)," Unpublished doctoral thesis, Princeton Univ. (Univ. Microfilms, Ann Arbor, Mich.). STEBBINS, W. C. (1966). "Auditory Reaction Time and the Derivation of Equal Loudness Contours for the Monkey," J. Exp. Anal. Behavior 7, 135. STEBBINS, W. C. "Hearing," in Behavior of Nonhuman Primates, A.M. Schrier and F. Stollnitz, Eds. (to be published), Vol. 3. SXEBBtNS, W. C., GREEN, S., and MtLLER, F. L. (1966). "Auditory Sensitivity of the Monkey," Science 153, 1646-1647. VER•ON, J. (1967). "Hearing in Subhuman Primates," Primate News 5, 4-11. WENDX, G. R. (1934). "Auditory Acuity of Monkeys," Comp. Psychol. Monograph 10, 1-51. WEVER, E.G., VERNON, J. A., and LAWRENCE, M. (1958). "The Nature of the Cochlear Potentials in the Monkey," Acta Oto-laryngol. 49, 87-92.



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pure-tone auditory behavioral thresholds in three species of lemurs

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