The ability of three species of birds to discriminate among selected harmonic complexes with fundamental frequencies varying from 50 to 1000 Hz was examined in behavioral experiments. The stimuli were synthetic harmonic complexes with waveform shapes altered by component phase selection, holding spectral and intensive information constant. Birds were able to discriminate between waveforms with randomly selected component phases and those with all components in cosine phase, as well as between positive and negative Schroeder-phase waveforms with harmonic periods as short as 1–2 ms. By contrast, human listeners are unable to make these discriminations at periods less than about 3–4 ms. Electrophysiological measures, including cochlear microphonic and compound action potential measurements to the same stimuli used in behavioral tests, showed differences between birds and gerbils paralleling, but not completely accounting for, the psychophysical differences observed between birds and humans. It appears from these data that birds can hear the fine temporal structure in complex waveforms over very short periods. These data show birds are capable of more precise temporal resolution for complex sounds than is observed in humans and perhaps other mammals. Physiological data further show that at least part of the mechanisms underlying this high temporal resolving power resides at the peripheral level of the avian auditory system.

1.
ANSI (1989). ANSI S3.6-1989, “Specifications for audiometers” (American National Standards Institute, New York).
2.
Brainard
,
M. S.
, and
Doupe
,
A. J.
(
2001
). “
Postlearning consolidation of birdsong: stabilizing effects of age and anterior forebrain lesions
,”
J. Neurosci.
21
,
2501
2517
.
3.
Carr, C. E., and Code, R. A. (2000). “The central auditory system of reptiles and birds,” in Comparative Hearing: Birds and Reptiles, edited by R. J. Dooling, A. N. Popper, and R. R. Fay (Springer-Verlag, New York), pp. 197–248.
4.
Carr
,
C. E.
, and
Friedman
,
M. A.
(
1999
). “
Evolution of time coding systems
,”
Neural Comput.
11
,
1
20
.
5.
Dooling, R. J. (1982). “Auditory perception in birds,” in Acoustic Communication in Birds, Vol. 1, edited by D. E. Kroodsma and E. H. Miller (Academic, New York), pp. 95–130.
6.
Dooling
,
R. J.
, and
Haskell
,
R. J.
(
1978
). “
Auditory duration discrimination in the parakeet (Melopsittacus undulatus)
,”
J. Acoust. Soc. Am.
63
,
1640
1643
.
7.
Dooling
,
R. J.
, and
Searcy
,
M. H.
(
1981
). “
Amplitude modulation thresholds for the parakeet (Melopsittacus undulatus)
,”
J. Comp. Physiol.
143
,
383
388
.
8.
Dooling
,
R. J.
, and
Searcy
,
M. H.
(
1985
). “
Temporal integration of acoustic signals by the budgerigar (Melopsittacus undulatus)
,”
J. Acoust. Soc. Am.
77
,
1917
1920
.
9.
Dooling, R. J., Lohr, B., and Dent, M. L. (2000). “Hearing in birds and reptiles,” in Comparative Hearing: Birds and Reptiles, edited by R. J. Dooling, A. N. Popper, and R. R. Fay (Springer-Verlag, New York), pp. 308–359.
10.
Dooling
,
R. J.
,
Dent
,
M. L.
,
Leek
,
M. R.
, and
Gleich
,
O.
(
2001
). “
Masking by harmonic complexes in three species of birds: Psychophysical thresholds and cochlear responses
,”
Hear. Res.
152
,
159
172
.
11.
Farabaugh, S. M., and Dooling, R. J. (1996). “Acoustic Communication in Parrots: Laboratory and Field Studies of Budgerigars, Melopsittacus undulatus,” in Ecology and Evolution of Acoustic Communication in Birds, edited by D. E. Kroodsma and E. H. Miller (Cornell U.P., Ithaca, NY), pp. 97–117.
12.
Fay, R. R. (1988). Hearing in Vertebrates: A Psychophysics Databook (Hill-Fay, Winnetka, IL).
13.
Fee
,
M. S.
,
Shraiman
,
B.
,
Pesaran
,
B.
, and
Mitra
,
P. P.
(
1998
). “
The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird
,”
Nature (London)
395
,
67
71
.
14.
Gleich, O., and Manley, G. A. (2000). “The hearing organ of birds and crocodilia,” in Comparative Hearing: Birds and Reptiles, edited by R. J. Dooling, A. N. Popper, and R. R. Fay (Springer-Verlag, New York), pp. 70–138.
15.
Goldstein
,
J. L.
(
1967
). “
Auditory spectral filtering and monaural phase perception
,”
J. Acoust. Soc. Am.
41
,
458
479
.
16.
Greenewalt, C. H. (1968). Bird Song: Acoustics and Physiology (Smithsonian Institute, Washington, DC).
17.
Guttinger
,
H. R.
,
Wolffgramm
,
J.
, and
Thimm
,
F.
(
1978
). “
The relationship between species specific song programs and individual learning in songbirds: A study of individual variation in songs of canaries, greenfinches, and hybrids between the two species
,”
Behaviour
65
,
241
262
.
18.
Heffner
,
R.
, and
Heffner
,
H.
(
1988
). “
Sound localization and the use of binaural cues in the gerbil
,”
Behav. Neurosci.
102
,
422
428
.
19.
Janata
,
P.
, and
Margoliash
,
D.
(
1999
). “
Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system
,”
J. Neurosci.
19
,
5108
5118
.
20.
Klump
,
G. M.
, and
Maier
,
E. H.
(
1989
). “
Gap detection in the starling (Sturnus vulgaris), I: Psychophysical thresholds
,”
J. Comp. Physiol.
164
,
531
539
.
21.
Kohlrausch
,
A.
, and
Houtsma
,
A. J. M.
(
1992
). “
Pitch related to spectral edges of broadband signals
,”
Philos. Trans. R. Soc. London, Ser. B
336
,
375
381
.
22.
Konishi
,
M.
(
1969
). “
Time resolution by single auditory neurons in birds
,”
Nature (London)
222
,
566
567
.
23.
Kroodsma, D. E., and Miller, E. H. (1982). Acoustic Communication in Birds, Vol. 2 (Academic, New York).
24.
Kroodsma, D. E., and Miller, E. H. (1996). Ecology and Evolution of Acoustic Communication in Birds (Cornell U.P., Ithaca, NY).
25.
Kuhl
,
P. K.
(
2000
). “
A new view of language acquisition
,”
Proc. Natl. Acad. Sci. U.S.A.
97
,
11850
11857
.
26.
Lavenex
,
P. B.
(
1999
). “
Vocal production mechanisms in the budgerigar (Melopsittacus undulatus): The presence and implications of amplitude modulation
,”
J. Acoust. Soc. Am.
106
,
491
505
.
27.
Leek
,
M. R.
,
Dent
,
M. L.
, and
Dooling
,
R. J.
(
2000
). “
Masking by harmonic complexes in budgerigars (Melopsittacus undulatus)
,”
J. Acoust. Soc. Am.
107
,
1737
1744
.
28.
Liberman
,
A. M.
,
Cooper
,
F. S.
,
Shankweiler
,
D. P.
, and
Studdert-Kennedy
,
M.
(
1967
). “
Perception of the speech code
,”
Psychol. Rev.
74
,
431
461
.
29.
Manley
,
G. A.
,
Gleich
,
O.
,
Oeckinghaus
,
H.
, and
Leppelsack
,
H.-J.
(
1985
). “
Activity patterns of cochlear ganglion neurones in the starling
,”
J. Comp. Physiol., A
157
,
161
181
.
30.
McGuirt
,
J. P.
,
Schmiedt
,
R. A.
, and
Schulte
,
B. A.
(
1995
). “
Development of cochlear potentials in the neonatal gerbil
,”
Hear. Res.
84
,
52
60
.
31.
Moss, C. F., and Simmons, J. A. (1996). “Perception along the axis of target range in the echolocating bat,” in Neuroethological Studies of Cognitive and Perceptual Processes, edited by C. F. Moss and S. J. Shettleworth (Westview, Boulder, CO), pp. 253–279.
32.
Patterson
,
R. D.
(
1987
). “
A pulse ribbon model of monaural phase perception
,”
J. Acoust. Soc. Am.
82
,
1560
1586
.
33.
Pumphrey, R. J. (1961). “Sensory Organs: Hearing,” in Biology and Comparative Anatomy of Birds, edited by A. J. Marshall (Academic, New York), pp. 69–86.
34.
Ryan
,
A.
(
1976
). “
Hearing sensitivity of the Mongolian gerbil
,”
J. Acoust. Soc. Am.
59
,
1222
1226
.
35.
Sachs
,
M. B.
,
Sinnott
,
J. M.
, and
Hienz
,
R. D.
(
1978
). “
Behavioral and physiological studies of hearing in birds
,”
Fed. Proc.
37
,
2329
2335
.
36.
Schroeder
,
M. R.
(
1970
). “
Synthesis of low-peak-factor signals and binary sequences with low autocorrelation
,”
IEEE Trans. Inf. Theory
16
,
85
89
.
37.
Schwartzkopff, J. (1968). “Structure and function of the ear and the auditory brain areas in birds,” in Hearing Mechanisms in Vertebrates, edited by A. V. S. De Reuck and J. Knight (Little, Brown, Boston), pp. 41–59.
38.
Sen
,
K.
,
Theunissen
,
F. E.
, and
Doupe
,
A. J.
(
2001
). “
Feature analysis of natural sounds in the songbird auditory forebrain
,”
J. Neurophysiol.
86
,
1445
1458
.
39.
Sinnott
,
J. M.
, and
Mosteller
,
K. W.
(
2001
). “
A comparative assessment of speech sound discrimination in the Mongolian gerbil
,”
J. Acoust. Soc. Am.
110
,
1729
1732
.
40.
Tchernichovski
,
O.
,
Mitra
,
P. P.
,
Lints
,
T.
, and
Nottebohm
,
F.
(
2001
). “
Dynamics of the vocal imitation process: How a zebra finch learns its song
,”
Science
291
,
2564
2569
.
41.
Theunissen
,
F. E.
, and
Doupe
,
A. J.
(
1998
). “
Temporal and spectral sensitivity of complex auditory neurons in the nucleus HVc of male zebra finches
,”
J. Neurosci.
18
,
3786
3802
.
42.
Vicario
,
D. S.
(
1991
). “
Contributions of syringeal muscles to respiration and vocalization in the zebra finch
,”
J. Neurobiol.
22
,
63
73
.
43.
Viemeister, N. F., and Plack, C. J. (1993). “Time analysis,” in Human Psychophysics, edited by W. A. Yost, A. N. Popper, and R. R. Fay (Springer-Verlag, New York), pp. 116–154.
44.
Yu
,
A. C.
, and
Margoliash
,
D.
(
1996
). “
Temporal hierarchical control of singing in birds
,”
Science
273
,
1801
2
.
45.
Zann
,
R.
(
1984
). “
Structural variation in the zebra finch distance call
,”
Z. Tierpsychol.
66
,
328
345
.
This content is only available via PDF.
You do not currently have access to this content.