Abstract
The distribution of frequencies along the basilar papilla of the barn owl (Tyto alba) was studied by labelling small groups of primary auditory neurones of defined frequency response and tracing them to their peripheral innervation sites. The exact location of marked neurones was determined in cochlear wholemounts with the aid of a special surface preparation technique. The average basilar papilla length (in fixed, embedded specimens) was 10.74 mm.
The resulting frequency map shows the basic vertebrate pattern with the lowest frequencies represented apically and increasingly higher frequencies mapped at progressively more basal locations. However, the length of basilar papilla devoted to different frequency ranges, i.e. the space per octave, varies dramatically in the barn owl. The lower frequencies (up to 2 kHz) show values between about 0.35 and 1 mm/octave, which are roughly equivalent to values reported for other birds. Above that, the space increases enormously, the highest octave (5–10 kHz) covering about 6 mm, or more than half of the length of the basilar papilla.
Such an overrepresentation of a narrow, behaviourally very important frequency band is also seen in some bats, where it has been termed an acoustic or auditory fovea.
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Abbreviations
- CF:
-
characteristic frequency
- HRP:
-
horseradish peroxidase
- NA:
-
Nucleus angularis
- NM:
-
Nucleus magnocellularis
References
Carr CE, Konishi M (1990) A circuit for detection of interaural time differences in the brain stem of the barn owl. J Neurosci 10:3227–3246
Coles RB, Guppy A (1988) Directional hearing in the barn owl (Tyto alba). J Comp Physiol A 163:117–133
Dooling RJ (1992) Hearing in birds. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing, Springer, New York, pp 545–559
Fay RR (ed) (1988) Hearing in vertebrates: A psychophysics databook. Hill-Fay Associates, Winnetka, Illinois
Fischer FP (1992) Quantitative analysis of the innervation of the chicken basilar papilla. Hearing Res 61:167–178
Fischer FP, Köppl C, Manley GA (1988) The basilar papilla of the barn owl Tyto alba: A quantitative morphological SEM analysis. Hearing Res 34:87–102
Fischer FP, Singer I, Miltz C, Manley GA (1992) Morphological gradients in the starling basilar papilla. J Morphol 213:223–240
Freeman DM, Weiss TF (1990) Hydrodynamic analysis of a two-dimensional model for micromechanical resonance of freestanding hair bundles. Hearing Res 48:37–68
Gleich O (1989) Auditory primary afferents in the starling: Correlation of function and morphology. Hearing Res 37:255–268
Greenwood DD (1990) A cochlear frequency-position function for several species — 29 years later. J Acoust Soc Am 87:2592–2605
Knudsen EI, Konishi M (1979) Mechanisms of sound localization in the barn owl (Tyto alba). J Comp Physiol 133:13–21
Knudsen EI, Blasdel GG, Konishi M (1979) Sound localization by the barn owl (Tyto alba) measured with the search coil technique. J Comp Physiol 133:1–11
Konishi M (1973) How the owl tracks its prey. Am Sci 61:414–424
Konishi M (1986) How auditory space is encoded in the owl's brain In: Cohen MJ, Strumwasser F (eds) Communication in the nervous system. John Wiley & Sons New York, pp 335–349
Köppl C, Manley GA (1989) An unusual frequency map in the inner ear of European lizards. Abstr 12th Midw Meetg ARO, St Petersburg Bch, Fla, pp 177
Köppl C, Manley GA (1990) Peripheral auditory processing in the bobtail lizard Tiliqua rugosa. II. Tonotopic organization and innervation pattern of the basilar papilla. J Comp Physiol A 167:101–112
Kössl M, Vater M (1985) The cochlear frequency map of the mustache bat, Pteronotus parnellii. J Comp Physiol A 157:687–697
Kössl M, Vater M (1990) Resonance phenomena in the cochlea of the mustache bat and their contribution to neuronal response characteristics in the cochlear nucleus. J Comp Physiol A 166:711–720
Lewis ER, Leverenz EL, Bialek WS (1985) The vertebrate inner ear. CRC Press, Florida
Liberman MC (1982) The cochlear frequency map for the cat: Labeling auditory nerve fibers of known characteristic frequency. J Acoust Soc Am 72:1441–1449
Manley GA (1990) Peripheral hearing mechanisms in reptiles and birds. Springer, Berlin Heidelberg New York
Manley GA, Gleich O (1992) Evolution and specialization of function in the avian auditory periphery. In: Webster DB, Fay RR, Popper AN (eds) The evolutionary biology of hearing. Springer, Berlin Heidelberg New York, pp
Manley GA, Brix J, Kaiser A (1987) Developmental stability of the tonotopic organization of the chick's basilar papilla. Science 237:655–656
Manley GA, Gleich O, Kaiser A, Brix J (1989a) Functional differentiation of sensory cells in the avian auditory periphery. J Comp Physiol A 164:289–296
Manley GA, Köppl C, Yates GK (1989b) Micromechanical basis of high-frequency tuning in the bobtail lizard. In: Wilson JP, Kemp DT (eds) Cochlear mechanics — structure, function and models. Plenum Publ Corp, New York, pp 143–151
Moiseff A (1989) Binaural disparity cues available to the barn owl for sound localization. J Comp Physiol A 164:629–636
Müller M (1991) Frequency representation in the rat cochlea. Hearing Res 51:247–254
Palmer AR, Russell IJ (1986) Phase-locking in the cochlear nerve of the guinea-pig and its relation to the receptor potential of inner hair-cells. Hearing Res 24:1–15
Patuzzi RB, Yates GK (1987) The low frequency response of inner hair cells in the guinea pig cochlea: Implications for fluid coupling and resonance of the stereocilia. Hearing Res 30:83–98
Payne RS (1971) Acoustic location of prey by barn owls (Tyto alba). J Exp Biol 54:535–573
Pollak GD, Bodenhamer RD (1981) Specialized characteristics of single units in inferior colliculus of mustache bat: Frequency representation, tuning, and discharge patterns. J Neurophysiol 46:605–620
Quine DB, Konishi M (1974) Absolute frequency discrimination in the barn owl. J Comp Physiol 93:347–360
Robertson D (1984) Horseradish peroxidase injection of physiologically characterized afferent and efferent neurones in the guinea pig spiral ganglion. Hearing Res 15:113–121
Schermuly L, Klinke R (1990) Origin of infrasound sensitive neurones in the papilla basilaris of the pigeon: An HRP study. Hearing Res 48:69–78
Schwartzkopff J, Winter P (1960) Zur Anatomie der Vogelcochlea unter natürlichen Bedingungen. Biol Zbl 79:607–625
Smith CA, Konishi M, Schuff N (1985) Structure of the barn owl's (Tyto alba) inner ear. Hearing Res 17:237–247
Smolders JWT, Ding D, Klinke R (1990) Gradients of functional properties of hair cells on the basilar membrane of the pigeon. In: Elsner N, Roth G (eds) Brain — perception — cognition. G Thieme, Stuttgart, New York, pp 125
Smolders JWT, Ding D, Klinke R (1992) Normal tuning curves from primary afferent fibres innervating short and intermediate hair cells in the pigeon ear. In: Cazals Y, Demany L, Horner K (eds) Auditory physiology and perception. Pergamon Press, Oxford, pp 197–204
Suga N, Neuweiler G, Moller J (1976) Peripheral auditory tuning for fine frequency analysis by the CM-FM bat, Rhinolophus ferrumequinum. IV. Properties of peripheral auditory neurons. J Comp Physiol 106:111–125
Sullivan WE (1985) Classification of response patterns in cochlear nucleus of barn owl: Correlation with functional response properties. J Neurophysiol 53:201–216
Sullivan WE, Konishi M (1984) Segregation of stimulus phase and intensity coding in the cochlear nucleus of the barn owl. J Neurosci 4:1787–1799
Vater M, Feng AS, Betz M (1985) An HRP-study of the frequencyplace map of the horseshoe bat cochlea: Morphological correlates of the sharp tuning to a narrow frequency band. J Comp Physiol A 157:671–686
Warchol ME, Dallos P (1990) Neural coding in the chick cochlear nucleus. J Comp Physiol A 166:721–734
Weiss TF, Rose C (1988) Stages of degradation of timing information in the cochlea: A comparison of hair-cell and nerve-fiber responses in the alligator lizard. Hearing Res 33:167–174
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Köppl, C., Gleich, O. & Manley, G.A. An auditory fovea in the barn owl cochlea. J Comp Physiol A 171, 695–704 (1993). https://doi.org/10.1007/BF00213066
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DOI: https://doi.org/10.1007/BF00213066