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01812

Frequency discrimination in the European starling (Sturnus A comparison of different measures

dgaris):

Ulrike Langemann and Georg M. Klump f nstitur j’iir Zootoc~ic, Tcchni.sctw (Received

Frequency-differericc frequency

limens CDL)

ch;lnge. Four different

sinuhoidai sweep upward extended

(type SSUf starting

frequency (type SSFM).

the

for pulsed

frequencies

of

I

frequency of

2 40 Hz (1S.Y Hz

for pulsed tonss. Furthermore, those at low modulation (27.7 Hz for type FSU, modulation

in a songbird. the European

Frequency

D1.s at two reference higher

SSU.

and

modulation

DLs

Only at high modulation

similar effects of stimulus type and reference

modulated

frequencies

frequencies

f’requencies

of 4 kHz. the differences

tone\ (type Fill), frequrncy

of srimulus of 33)

that

ostcnding to both hide5

1 kHz. the starling ahowed rn(~dul~ltion at rn(~~lLll~ltion

type ASFM).

At a rrtrcnce

( 40 Hz was about twice as large (>I.6

frequency

a single

modulation

Hr.1 than

Hr wc’rc ahout twice ;1s large a\

in the DLh for various stimulus types were insignificant

and low modulation

f’requencies,

were the I1Ls increased.

on the frequency-difference

sinuso&l

and ~Isyrnrn~trl~~~l t’rrqucncy

signals at ;I modulation

( 2 370 Hz)

periodic

for stimuli dil’fcring in the type of pulxd

1 :~ntl=ikHz. were xtudicti. At

frequencies,

at modulation

between

sinusoidal frequency modulation

15.3 Hz for low modulatton

frequency

frequency

periodical

for single \wrrps

(type SSFM)

the DLs for periodically At a reference

and a symmetrical

23.3 Hz for type SSU. 28.0 Hz for type ASFM

frequencies).

in frequency

in the center of an X00 ms signal. an asymmetrical

for stimulus

frequencies.

C;trrchrrrg, FR(G

starling t.S~n~a~ w/guri.r),

change were studied: an increase

tones 11 1.3 1%~). slightly

kHz, the DL for symmetrical

Llr~ic~c~rsirij~Miinc/w~,

1902: Revision received and accepted 3 June lYY2)

frequency (type ASFM),

of the rel’crence DL

determined

werr

type5 of freyuency

only ahove the reference

lowest

6 January

and 24.6 H/

The result\

for type SSFM

and low

arc discussed with respect to

limen in humans and with respect to the t’rrquency

DLh in

other bird species.

Frequency-diilerence

limen: Frequency

resolution:

Starling:

Bird

Introduction In humans, the size of the frequency-difference limen depends on the way in which the frequency change occurs. At frequencies below about 4 kHz, the frequency-difference limen that is determined using pulsed tones (difference limen for frequency, DLF, Moore, 1989) is much smaller than the difference limen determined by using sinusoidally frequency-modulated signals (termed frequency-modulation difference limen, FMDL, Moore, 19891. This effect cannot he the result of procedurat differences between the different studies reviewed by Moore (19891, since it is also found when the same subjects are tested with identical procedures under the two different conditions (see Fastl, 1978; Schorer, 1989a,b; Moore and Glasberg, 1989; Demany and Semal, 1989). Schorer (1989b) introduced a third type of frequency change that contained a single upward variation in frequency starting with a constant frequency tone and ending with a

~~~~~~s~~~~~~~~z~,~, fo: Georg

the

M. Klump,

Univ~rsit~~t Miinchen,

FRC;. Fax: (4V) 89-3209-2727.

institut

Licht~nb~rgst~~ss~

fiir Zoologie.

4, D-8046

TechnisGarching.

constant frequency tone. The freq~lency-differeffce Iimen determined with this third stimulus type was intermediate between the DLF and the FMDL. At high frequencies (e.g. 4 to 8 kHz) the difference in the size of the DL with the type of presentation of the frequency change vanished (Fastl, 1978; Demany and Semal, 19891, or may even be reversed (see comparison of results from different studies by Wier et al., 1977). The mechanism underlying this variation in the frequency-difference limen with the type of frequency change is unclear. An animal model that shows the effect described in humans may bring us closer to its understanding. The purpose of this study is to test whether the European starling, a songbird that serves as a model for many aspects of auditory processing, shows perceptual differences in frequency discrimination similar to those in humans. For birds in general, frequency (i.e., the perceived pitch) and the change in frequency (e.g., commonly found as sinusoidal frequency modulation in their song, see Greencwalt, 1968) are among the most salient parameters used in species and individual recognition of song (e.g. Nelson, 1988; Nelson and Marler, 1990; Weary, 1990; Hurley et al., 1990). In the European starling, ‘frequency modulated song elements are

widespread and play an important role in species and individual recognition (e.g., see Adret-Hausberger. 1989). Thus, birds like the starling should have evolved efficient mechanisms for the analysis of frequency and frequency change that are tested in the experiments reported below. Contrary to humans, however, in birds pitch is preferentially processed as absolute pitch and not as relative pitch (e.g., see Dooling et al., 1987; Page et al., 19891, although some bird species either naturally also show relative pitch perception (e.g., see Hurley et al., 1990) or can be trained to use relative pitch and not the frequency of the stimulus in discrimination experiments (e.g. the starling, see Page et al., 1989, and the review by Hulse, 1989). The phenomenon of virtual pitch can also be demonstrated in the starling by the perception of missing fundamentals (Cynx and Shapiro, 1986).

varied in steps of 0.375 dB by a custom-built attenuator (Analog Devices AD 7111) under the control of the microcomputer. The signals were amplified (Yamaha A-520), and fed into a speaker (Heco KCS2,590 Hz- 14 kHz, k5 dB). The speaker was mounted 40 cm from the position of the birds’ head at about 0 degree elevation. Sound pressure levels were calibrated (Gcnera1 Radio type 1982 sound-level meter) at least once per day by mounting the 1”-condenser microphone at about the position where the bird’s head would be during the experiment. The total harmonic distortion of sine-wave stimuli presented through the complete sound system was less than 0.2% (recorded through the General Radio sound-level meter with the l”-condenser microphone attached and analyzed with a HP 356i Dynamic Signal Analyzer). Stimuli

Materials and Methods Subjects

Four European starlings (two females: We, Co, and two males: Bl, Ro) between 2 and 5 years old were used. The birds were kept individually in cages of 80 x 40 X 40 cm3 with a natural day/night cycle. The birds were tested on five to seven days per week. During the testing, food intake outside the experimental sessions was restricted so that the birds were between 90 and 95% of their free-feeding weight. Three of the birds (We, Ro, Bl) had been used in a previous psychoacoustical experiment on gap detection (JUump and Maier, 1989). All four birds previously were subjects in a study on temporal modulation transfer functions of broadband signals (Klump and Okanoya, 1991) and on the detection of amplitude modulation in pure tone signals (JUump, submitted). Apparatus

Details of the behavioral apparatus have been given elsewhere (Khrmp and Maier, 1989) and only a brief description is given here. The experimental cage was placed in a sound proof box. On the front wall of the cage, two response keys (observation key and report key) with an attached light-emitting diode (LED) and a photo-interrupting switch were mounted. The bird could peck the keys to indicate a response. A rotary food dispenser operated by a stepping motor was placed in front of the cage. The bird was able to pick a piece of mealworm from the dispenser for each reinforcement. The behavioral protocols were controlled by an IBM-AT compatible microcomputer. All signals were produced by an eight-bit digital-toanalog (D/A) converter at a sampling rate of 25 kHz via a 6 kHz low-pass filter for anti-aliasing Nrohn Hite 3202, 48 dB/octave). The signal amplitude could be

The different stimuli with the variation in the signal frequency are shown in Fig. 1. The reference stimuli against which those stimuli had to be discriminated consisted of pure tones of 1 or 4 kHz. All stimuli had a total duration of 800 ms and a linear rise and fall of 8 ms (other durations used in the experiments are mentioned specifically) and were presented at a regular rate of 1 stimulus every 1.6 s. They were presented at an average SPL of 61 dB which in the starling at 1 and 4 kHz corresponds to a sensation level of about 50 dB (median auditory thresholds measured in our setup with starlings from our colony were 10 and 11 dB SPL at 1 and 4 kHz, respectively; see Baur, 1989; for other threshold estimates in the starling see Dooling et al., 1986; Kuhn et al., 1982). The amplitude of the stimuli was randomized from one stimulus to the next in the range of +3 dB in steps of 0.375 dB (the switching occurred in the silent gap between the stimuli). This randomization was used to prevent the birds from possibly using perceived loudness changes with the change in frequency (see Moore and Glasberg, 1989; they have shown in humans that the frequency-difference limens measured with a randomization of signal level over a range of 6 dB were only 15% larger than those measured with the level fixed). Four different types of stimuli with a variation in the signal frequency were applied in the experiments. The first stimulus type (frequency step upward: FSU) consisted of two tones of 400 ms duration separated by a silent gap (Fig. la). The first tone always was of the reference frequency, and the second tone had a higher frequency (in the case of a reference stimulus its frequency was identical to that of the first tone). The durations of the gap as measured at the half-power points of the signal envelope were 8, 25 or 100 ms. They were chosen such that they were similar in duration to that of the frequency-sweep part of the second stimulus type. This second type (Fig. lb; single sweep

45

a

Reference

and 320 Hz (i.e., the sweep durations for a half-wave were 100, 25, 6.25 and 1.56 ms; see also the durations of the silent gaps in stimulus type FSU). The third and fourth stimulus types consisted of periodically frequency-modulated tones. In the case of the third type, the modulation was asymmetrical with respect to the reference frequency; it only extended upward from the reference frequency (Fig. lc; asymmetrical sinusoidal frequency modulation: ASFMl. The fourth stimulus type, was the ‘standard’ sinusoidal frequency modulation, which is symmetrical with respect to the reference frequency such that the total range of frequency change (here always expressed by the term ‘frequency excursion’1 is twice the maximum deviation from the reference frequency (Fig. Id; symmetrical sinusoidal frequency modulation: SSFM). The modulation frequencies used for the last two types of stimuli were 5, 10, 20, 40, 80, 160, 320 and 640 Hz. Except for the first stimulus type with a silent gap between the two parts, the reference stimulus to which the signal stimuli with a frequency change were to be compared was a single pure tone of the reference frequency and with a similar duration and envelope.

Frequency

Time

Reference

Frequency

Time

Reference

Frequency

Procedures Time

..,....

Reference

Frequency

LTime Fig.

I. Schematical

a) frequency

experiments: step upward, quency;

sonagrams

FSU),

of the different

increment

the first tone

b) single sweep

upward

stimuli

with pulsed consisted

WLJ)

of the reference

in frequency,

sweep the tone consisted of the reference

frequency,

the form of a sinusoid, and the maximum

deviation

ence frequency cal sinusoidal ence frequency the frequency reference 6SFMf frequency,

remained frequency

span is equal

extending

fre-

to the

the sweep had from the refer-

(ASFM)

starting

at the refer-

only above the reference to the maximum

d) symmetrical symmetrically

the frequency

prior

until the end of the stimulus; c) asymmetrimodulation

and extending

frequency;

used in the

tones (frequency

deviation

sinusoidal frequency below

above

from

the

modulation

the

reference

span is two times the maximum

deviation

from the reference

and

frequency.

frequency.

upward: SSU> consisted of two tones as in the first type. However, they were connected by a frequency sweep in the form of a half-wave sinusoid. The rate of frequency change determined by the form of the sinusoid was identical to the rate of change in some of the periodically modulated stimuli described below and corresponded to modulation frequencies of 5, 20, 80

A GO/NOGO procedure with a repeating-background (Okanoya and Dooling, 1990) was used to measure the various frequency-difference limens of the starling. The birds were trained to peck an observation key continuously when pure tones without a frequency change (background) were repeated and to peck a second report key when a stimulus with a change in frequency (signal) was presented. A variable interval timer started when the bird first pecked the obsetvation key. After a random waiting interval of between 1 and 7 s, another peck on the observation key lead to the replacement of one background stimulus by a signal stimulus with a certain frequency excursion. If the bird pecked the report key within 3 s from the presentation of the signal with the changing frequency, the food tray rotated and the bird was reinforced with a piece of mealworm with a probability of 80% (this reinforcement schedule ensured that the capacity of the feeder was sufficient for the total session). A feeder-light was always presented as a secondary reinforcer. To obtain a measure of spontaneous responding, a catch trial during which no frequency change (the repeated-background reference tone) occurred was inserted on 30% of the trials. A response on the report key during a catch trial or during a waiting interval was punished by a timeout period of between 4 and 20 s with the lights in the experimental cage switched off. The length of timeout period was manipulated in order to control the false-alarm rate of the birds. Frequency-difference limens were obtained by the method of constant stimuli. A block of 10 trials, con-

sisting of 3 catch trials (no frequency change) and a set of 7 signal trials (all with the same type of frequency change, but differing frequency excursion), was repeated ten times in a session with a randomized sequence of the trials. At the beginning of each run, a warm-up block of ten trials with a frequency excursion was presented that could be easily detected by the birds. If the bird did not complete 100 trials required to finish a session in a single run, but finished 20 triafs or more, the data were saved and remaining trials were presented in a subsequent run. If the false alarm rate of a run exceeded 20% or if the two signals of the set with a frequency excursion well above the starlings’ difference limen were reported with a probability of less than 80%, that run was discarded. Within one session, only one type of frequency change and one reference frequency were presented. Estimation of the frequency-difference

limen

A psychometric function for one stimulus type based on 10 triaIs at each frequency excursion and 30 catch trials was constructed at the conclusion of a session.

a

The frequency-difference limen was then computed bq linear interpolation as the frequency excursion at which the index of detectability d’ (see Swets. 1964) was 1.X (in the case of the starlings’ typical false-alarm rate this corresponds to about 50% correct reports in this GO/NOGO task). Close to the final frequency-difference limen, the Weber fractions corresponding to the various frequency excursions differed by no more than 0.01, often this difference was only 0.003. Two sessions of 100 trials each were combined for a final estimate of the difference limen that was then based on 20 trials at each frequency excursion and 60 catch trials, but only if the two subsequent estimates of the difference limens in those two sessions collected in succession differed by no more than 20% from each other (this corresponds to a difference in Weber fraction that was always smaller than 0.01; in the majority of cases, it was less than 0.003). Within an experimental series for the estimation of the frequency-difference limens for one type of stimulus (e.g. FSU, SSFM, etc.). but with varying parameters (e.g. size of the silent gap, modulation frequency etc.),

b

50

1kHz

45

50 45.

72 =*o I

g40. G 35 3; 30 g 25

1;::

I..-___++

51 8

25

100

Gap [ms]

5

5

20

80

Modulation

320

Frequency

'-

[Hz]

d

C 50

50 I 45

5'

5

10

20

Modulation

40

80

160

Frequency

320

[Hz]

640

5’

I

5

10

20

Modulation

40

80

160

Frequency

320

640

[Hz]

Fig. 2. Frequent-difference iimen for a reference frequency of 1 kHz; median values and ranges of four subjects: af frequency increment using pulsed tones (FSU); b) single sweep upward in frequency (SSU); cf asymmetrical sinusoidal frequency modulation (ASFM); d) symmelrical sinusoidal frequency modulation (SSFM).

the sequence of variation of these parameters was randomized individually for each bird. To exclude the possibility that improved detection during the time course of an experimental series would occur and remain undetected, at the end of each series the difference limen for the parameter setting used first in the series was redetermined. Only if the two difference limens were within the limits set for the combination of sessions, the series was concluded. Otherwise, the testing with subsequent parameters continued until this criterion of longterm stability of the difference limen was reached. Only the data recorded for each parameter setting in the final 200 trials are reported here, since these data would be based on the largest experience of the birds with the particular stimulus (i.e., all trials prior to the final 200 trials were treated as training rather than test trials). First, all experiments at a reference frequency of I kHz were completed, then testing continued at a reference frequency of 4 kHz, since initially all birds showed problems in transferring the detection of frequency change to a new reference frequency. Repeat measurements at 1 k&z after the completion of the 4 kHz series showed that the birds did not significantly increase their performance during the time course of experimentation (altogether Y months).

Results The data reported here are the result of 1,350 sessions (including all controls) with a total of 148,500 signal trials. 3.3% of all sessions had to be exciuded from the analysis, because the individual’s false-alarm rate exceeded 20% and 3.7% of the sessions were not used, because the subject did not report the correct detection of the two signals with a frequency excursion that was well above the difference limen with a probability that was larger than 80%. The average false-alarm rate of the birds in the sessions on which the data reported below are based was 5. I % (the range was 0 to 11.7%).

The smallest frequency-difference limens at 1 kHz in the starling were found for frequency increments of pulsed tones (stimulus type FSU, Fig. 2a). The best difference limen was found when the two tones were separated by :I silent gap of 25 ms (best median value: 9.3 Hz; best individual performance 7.0 Hz). Overall, the median difference limen for pulsed tones was 11.4 Hz. For the stimulus with a single frequency sweep upward (type SSU, Fig. 2b) and sweep durations corresponding to the durations of the silent gaps, the difference limcn was slightly increased. The median values

for sweep durations of 100 ms (SSU, m~~dulation frequency 5 Hz) and gap durations of lOi, ms (FSU) were 14.8 and 11.1 Hz, respectively. For sweep durations of 25 ms (SSU, modulation frequency 20 Hz) and gap durations of 25 ms (FSU) the median values wcrc 15.0 and 9.3 Hz, respectively; and the results for the faster rates of modulation and the shortest gap pointed in the same direction (the overall median difference limen for this stimulus type was 15.Y Hz). In the case of sinusoidal modulation in only one direction from the reference frequency (type ASFM, Fig. 2~1, the median frequency-difference timens were very similar to those found for the stimulus type SSU when looking at low modulation frequencies (5 80 Hz). The diffcrcnce limens further increased at modulation frequencies of 160 and 320 Hz (maximum median difference limen 22.Y Hz), but again decreased at the highest modulation frequency of 640 Hz (median DL: 14.1 Hz). In the case of a sinusoidal frequency modulation that extends symmetrically to both sides of the reference frequency (type SSFM, Fig. 2d1, with the exception of the modulation frequency of X0 Hz, the frequency-difference limcn is further increased when compared to stimulus ASFM. The strongest decrease in performance is found at a modulation frequency of 320 Hz at which the median difference limen was 36.X Hz. As in the cast of stimulus ASFM, the performance of the birds improved very much at the highest modulation frequency tested (640 Hz). At low modulation frequcncics ( 2 40 Hz), the median difference limen for the stimulus type SSFM of 20.7 Hz was about twice as large as that mcasurcd for pulsed tones ( I 1.4 Hz, type FSU). A number of control experiments were conducted at the reference frequency of 1 kHz. First, we compared the birds’ performance for two different types of stimuli with a frequency step upward (type FSU) between pulsed tones. The introduction of a temporal gap between the tone pulses could be done while keeping the total stimulus duration of 800 ms constant and reducing the duration of the second tone pulse to a minimum of 300 ms at the largest gap duration of 100 ms, or by extending the total duration (these results are displayed in Fig. 2af. There were only small differences between the two types of FSU-stimuli. The frcqucncydifference limens measured for the stimuli with an extended total duration on average were 2.3 Hz (median of 12 values) better than those measured with a constant total duration. In a second control experiment we studied the effect of randomizing the signal amplitude from one stimulus to the next. Difference limens for four modulation frequencies (10. 40, 160. 640 Hz) in the stimulus type ASFM, and for all durations of the temporal gap in stimulus type FSU were compared when measured with and without a randomization in signai amplitude from one stimulus to the next. The frequency-difference limcns were 1.7 Hz (FSU. median

48

of 12 values) and 0.1 Hz (ASFM, median of 16 values) larger when measured without randomization of signal amplitude than with randomization of signal amplitude. The frequency-difference limen for different modes of frequency change at a reference frequency of 4 kHz

At a reference frequency of 4 kHz, the frequencydifference limen increased for stimulus type FSU with increasing size of the temporal gap from 19.0 Hz for the shortest gap (8 ms) to 35.8 Hz for the largest gap of 100 ms (all four individuals show this trend, Fig. 3a). Overall, the median difference limen for pulsed tones with all gap sizes included was 27.7 Hz. For single frequency sweeps upward (stimulus type SSU, see Fig. 3b) and sweep durations corresponding to the durations of the silent gaps in the stimulus type FSUj the overall median frequency-difference limen was 23.8 Hz. At low modulation frequencies (5 80 Hz) with both symmetrical and asymmetrical modulation, the median frequency-difference limens were relatively similar (28.0 Hz for type ASFM, median of 20 values,

a

for differences between modulation frequencies see Fig. 3c; 24.6 Hz for type SSFM, median of 20 values, for differences between modulation frequencies see Fig. 3d). Only at high modulation frequencies of 320 Hz and 640 Hz were the values of the difference limen larger than at low modulation frequencies. At a modulation frequency of 320 Hz, the median frequency-difference limens for the stimuli ASFM and SSFM were 58.6 Hz and 87.6 Hz, respectively. The drop in the frequency-difference limen at a modulation frequency of 640 Hz was not as large as in the case of the reference frequency of 1 kHz where the values for the difference limen again came close to those for low modulation rates. At 4 kHz, the median difference limens for a modulation frequency of 640 Hz were 48.0 Hz and 68.8 Hz for the stimulus types ASFM and SSFM, respectively. At 4 kHz, another control experiment was conducted to study the effect of shortening the second tone pulse in the stimulus type FSU when the size of the temopral gap was increased (the data reported above were gathered with the second tone pulse ex-

b

m80_ 4kHz 2 -70 $60. ;3

Ii;:

;-II

rn __

101

100

6

Gapz;lns]

A

5

20

Modulation

80

320

Frequency

[Hz]

d

C

90

90

t

t

101

10' 5

10

20

Modulation

40

80

1130 320

Frequency

[Hz]

840

5

160

M$u&ob°Fre~ency

320

640

[Hz]

Fig. 3. Frequency-difference limen for a reference frequency of 4 kHz; median values and ranges of four subjects: a) frequency increment using pulsed tones (FSU); b) single sweep upward in frequency (SSU); c) asymmetrical sinusoidal frequency modulation (ASFM); d) symmetrical sinusoidal frequency modulation (SSFM).

‘49

tended to 400 ms, irrespective of the size of the gap). The frequency-difference limens measured for the FSU-stimuli with an extended total duration on average were 1.6 Hz (median of I2 values) worse than those measured with a constant total duration of the stimulus of 800 ms. Thus, as in the corresponding control experiment at 1 kHz the effects of shortening the second pulse to a minimum of 300 ms when increasing the size of the temporal gap were insignificant.

Discussion

The primary goal of this study was to find out whether the European starling is a suitable animal model in the study of frequency discrimination that displays a variation in the frequency-difference limens for different modes of frequency change similar to that found in humans. Our results show that the starling, indeed, may be suited as such an animal model for the perceptual effects found in humans. As in humans (e.g. see Fastl, 1978; Schorer, 1989a,b; Demany and Semal, 19891, at 1 kHz the frequent-difference limen is smallest when determined with pulsed tones (FSU), largest when determined with symmetrical sinusoidal modulation (SSFMI, and intermediate when determined with a single upward frequency sweep (SSU) or with asymmetrical sinusoidal modulation (ASFM). The differences between the frequency-difference limens for the various stimulus types are reduced at the carrier frequency of 4 kHz, which is similar to the results in humans (Fast& 1978; Demany and Semal, 1989). The difference between the frequency resolution in the starling’s auditory system measured with symmetrical sinusoidal modulation and that measured with asymmetrical sinusoidal modulation at a carrier frequency of 1 kHz suggests, that the starling (as was proposed for humans, see Schorer 1989b) may use two cues simultaneously in detecting the modulation. First, it may use the average deviation from the carrier frequency which is zero in the case of symmetrical modulation, but exists for the other three types of stimuli with a frequency change used in this study. The difference in the frequency resolution measured with the symmetrical and asymmetrical modulation at 1 kHz suggests that at this low carrier frequency the average deviation from the carrier frequency plays an important role. It does not seem to play a role for the starlings at 4 kHz, since no difference between the frequency discrimination measured with symmetrical and asymmetrical modulation is found. The second cue which the starlings may use is the size of the frequency excursion within the stimulus. This cue was similar for all four types of stimuli. The results in the starling at 4 kHz (i.e., no differences in the frequency resolution as

measured with the various stimulus types at low modulation frequencies) suggest, that this cue may play a dominant role at high carrier frequencies. Thus, the shift in the relative importance of the different available cues, i.e., the average deviation from the carrier frequency or the size of the frequency excursion, may explain the differences in frequency resolution found at 1 kHz, and also the similarity found at 4 kHz. Schorer (1989b) presented a model for the perception of different types of frequency change that incorporated two different pathways for the detection of the change in the signal’s frequency. The first pathway extracts the average pitch of the signal with a relatively long integration time (about 200 ms). The frequencydifference information generated by this pathway depends on the pitch difference between the signals and on their pitch strength (for a definition of pitch strength see Fastl, 1989, and Zwicker and Fastl, 1990; briefly, the pitch sensation cannot only be labelled as high or low, but also as faint or strong, i.e., assigned a pitch strength). The second pathway extracts the information on the signal’s pitch using the rapid variation in the excitation patterns in the cochlea (its time constants may be approximated by the time constants of modulation transfer functions). If the frequency-difference Iimen is smaller for the first pathway, the DLF should be smaller than the FMDL. If the frequency-difference limen is smaller for the second pathway, both DLF and FMDL should be similar (the two signals which are to be compared in the case of the DLF should not be separated too much in time, otherwise memory limitations may enlarge the DLF), since for both types of signals the maximum variation in the excitation pattern of the cochlea should be similar. If the first pathway evaluates a measure that is correlated with the ratio pitch (unit ‘mel’; ratio pitch scales are generated by having subjects judge halving or doubling of pitch with respect to a reference tone, see Zwicker and Fastl, 19901, then Schorer’s (1989b) model may explain why the DLF is much smaller than the FMDL at 1 kHz and both are similar at high frequencies. The ratio pitch is proportional to the signal frequency at low frequencies, but grows less than in proportion to the signal frequency at high frequencies, i.e., above 1 kHz a frequency increase by a constant Weber fraction in humans leads to a much smaller increase in the ratio pitch at high frequencies than at low frequencies (e.g. see Zwicker, 1982; Zwicker and Fastl, 1990). Thus, at high frequencies the sensitivity for frequency differences based on the cue involving ratio pitch would be diminished. Unfortunately, we do not have data on the ratio pitch in the European starling that would allow a test of this hypothesis. Schorer’s model may also be able to explain the result of Demany and Semal(1989) who found that for short duration tones (25 ms) the frequency dependence of the DLF is similar to that of

the FMDL for a slow rate of sinusoidal modulation (2 Hz). Fast1 (1989) has shown that short-duration tones have only a reduced pitch strength when compared to long signals. Since a small pitch strength leads to a reduced sensitivity for the detection of a frequency change in the first pathway in Schorer’s (1989b) model, the second pathway may determine the difference limen which then should be similar for both types of signals. The large increase in the discrimination thresholds found in the starling at a modulation frequency of 320 Hz in the case of sinusoidal modulation may be due to a lack of ability to code such rapid changes in frequency as is suggested by the results from a neurophysiological study on the starling’s auditory forebrain (Knipschild et al., 1992). Knipschild et al. (1992) found, that the ability of forebrain neurons to code sinusoidal frequency modulation by phase coupling to the modulation is reduced at such high modulation frequencies. The decrease in the difference limen at a modulation frequency of 640 Hz may result from an increased availability of spectral cues, since the spectral energy is no longer limited to one analysis channel (e.g. as characterized by the starling’s critical band) centered on the carrier frequency. Direct measurements of the starling’s critical bands are not yet available, but estimates can be made from its critical masking ratios (see Dooling et al., 1986; Langemann et al., 1992). If we assume that similarly to the results in the parakeet (Saunders et al., 1979) and in humans (Zwicker et al., 19571, also in the starling the size of the critcal band is about 2.5 times the bandwith described by the critical masking ratio, then the critical bandwidths would be 287 Hz and 1143 Hz at 1 and 4 kHz, respectively (based on median critical masking ratios of 6 starlings). At 1 kHz, the sidebands generated by the modulation frequency of 640 Hz would be located far outside the critical band centered at the carrier frequency. Thus, a very sensitive detection of the modulation might be explained by the birds using this spectral information. A computation of the spectrum at the FMDL revealed, that the starlings would be presented with a level of the sideband that should be just audible to them (i.e., less than 10 dB above their threshold of hearing). At 4 kHz, the sidebands located far outside the critical band centered at the carrier frequency are not audible to the starlings (the level is below the threshold of hearing in quiet). Thus, the sensitivity for the detection of the modulation might only be slightly improved by the birds using the spectral information of the first set of sidebands generated by the modulation (fcarrier - fmod; fcarrier+ fmod). Both for the 4-kHz-stimulus with 640 Hz sinusoidal modulation and the I-kHz-stimulus with 320 Hz sinusoidal modulation, at the FMDL the spectral sidebands., which might be used fo the detection of the modulation: are about 30 dB down with reference to

the level at the carrier frequency and are probably audible to the birds. A difference in the frequency resolution for differ.. ent stimulus types, i.e., for pulsed tones and symmetrical sinusoidal modulation, has also been dcscribcd in another bird species, the pigeon (Colurnbu tiriu, Brgucker and Schwartzkopff, 1986). In the pigeon, however, the frequency-difference limen was found to be larger if measured with pulsed tones than if measured with sinusoidal modulation (the range of modulation frequencies was 1.6 to 25 Hz). The discrimination thresholds reported by Braucker and Schwartzkopff (1986) for pure-tone stimuli were. however, much larger than those reported previously by Sinnott et al. (1980). Thus, it is questionable whether the unusual result in the pigeon found by BrCucker and Schwartzkopff (1986) was due to an enlarged DLF in their subjects instead of being due to the fact that the actual sensory thresholds were not approached in the experimental procedure used. The data on the starling’s frequency-difference limen for pure tones were almost identical to those measured in a previous study by Kuhn et al. (1980) if instead of a d’ of 1.8 a d’ of 1.0 was used as the threshold criterion. They also were very similar to the difference limens reported both for a number of mammals and other bird species (see data summary in Fay, 1988). Thus, the starling may be suitable as a general model for the study of frequency resolution in vertcbrates.

Acknowledgements

We thank R. Dooling and H. Fast1 for comments on a previous draft of the manuscript. A. Kiihler’s help in running the experiments is gratefully acknowledged. The study was supported by a grant from the Deutsche Forschungsgemeinschaft (Sonderforschungsbereich 204) and by a graduate student stipend (U.L.) from the Technical University, Munich.

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