Summary
The cochlea of the mustached bat (Pteronotus parnellii) has sharp tuning characteristics and pronounced resonance within a narrow band near the second harmonic, constant frequency (CF2) component of the animal's biosonar signals. That fine frequency discrimination occurs within this narrow band is evident from Doppler-shift compensation, whereby bats in flight lower the frequency of emitted CF2s to maintain returning echoes within this band. This study examined various factors capable of producing shifts in both the cochlear resonance frequency (CRF) and CF2s emitted by stationary bats and bats actively Doppler-shift compensating on a pendulum. Each of three experimental factors shifted the CRF in a reversible manner. Changes in body temperature produced an average CRF shift of 39 ± 18 Hz/°C. The CRF increased with flight by 150 ± 100 Hz and returned to baseline values within 10 min after flight. Contralateral sound exposure produced smaller (100 ± 20 Hz), rapid shifts in the CRF, suggesting that a mechanism different from the temperature- and flight-related shifts was involved. Changes in the CRF induced by temperature and flight were accompanied by shifts in the emitted CF2 of stationary and moving bats. Coupled with a companion study of associated shifts in neural tuning, the concomitant changes in CRF and CF2 provide evidence of cochlear tuning lability in the mustached bat.
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Abbreviations
- CF2:
-
second harmonic, constant frequency component of the biosonar signal
- CM:
-
cochlear microphonic
- CRF:
-
cochlear resonance frequency
References
Bell A (1992) Circadian and menstrual rhythms in frequency variations of spontaneous otoacoustic emissions from human ears. Hearing Res 58:91–100
Bishop AL, Henson OW Jr (1987) The efferent cochlear projections of the superior olivary complex in the mustached bat. Hearing Res 31:175–182
Brown AM (1988) Continuous low level sound alters cochlear mechanics: an efferent effect? Hearing Res 34:27–38
Brown CR, Bernard RTF (1991) Validation of subcutaneous temperature as a measure of deep body temperature in small bats. J Zool Lond 224:315–346
Covey E, Vater M, Casseday JH (1991) Binaural properties of single units in the superior olivary complex of the mustached bat. J Neurophysiol 66:1080–1094
Davis H (1983) An active process in cochlear mechanics. Hearing Res 9:79–90
De Boer E (1983 a) No sharpening? A challenge for cochlear mechanics. J Acoust Soc Am 73:567–573
De Boer E (1983 b) On active and passive cochlear models — toward a generalised analyis. J Acoust Soc Am 73:574–576
De Boer E (1983 c) Power amplification in an active model of the cochlea — short wave case. J Acoust Soc Am 73:577–579
Dijk P van, Wit HP (1987) Temperature dependence of frog spontaneous otoacoustic emissions. J Acoust Soc Am 82:2147–2150
Dijk P van, Wit HP, Segenhout JM (1989) Spontaneous otoacoustic emissions in the European edible frog (Rana esculenta): spectral details and temperature dependence. Hearing Res 42:273–282
Gaioni SJ, Riquimaroux H, Suga N (1990) Biosonar behavior of mustached bats swung on a pendulum prior to cortical ablation. J Neurophysiol 64:1801–1817
Gooler DM, O'Neill WE (1987) Topographic representation of vocal frequency demonstrated by microstimulation of anterior cingulate cortex in the echolocating bat, Pteronotus parnellii parnellii. J Comp Physiol A 161:283–294
Haggerty HS (1989) Spontaneous otoacoustic emissions: evidence for circadian rhythm of frequency variation. J Acoust Soc Am Suppl 86:S44
Haggerty HS (1990) Spontaneous otoacoustic emissions: evidence for a monthly rhythm of frequency variation in women. Assoc Res Otolaryngol Abstr 13:233
Henson MM (1973) Unusual nerve-fiber distribution in the cochlea of the bat, Pteronotus p. parnellii (Gray). J Acoust Soc Am 53:1739–1740
Henson MM (1978) The basilar membrane of the bat, Pteronotus p.parnellii. Am J Anat 153:143–157
Henson MM, Henson OW Jr (1991) Specializations for sharp tuning in the mustached bat: the tectorial membrane and spiral limbus. Hearing Res 56:122–132
Henson MM, Henson OW Jr, Goldman LJ (1977) The perilymphatic spaces in the cochlea of the bat, Pteronotus p. parnellii (Gray). Anat Rec 187:767
Henson MM, Henson OW Jr, Jenkins DB (1984) The attachment of the spiral ligament to the cochlear wall: anchoring cells and the creation of tension. Hearing Res 16:231–242
Henson OW Jr, Henson MM (1988) Morphometric analysis of cochlear structures in the mustached bat, Pteronotus parnellii parnellii. In: Nachtigall PE, Moore PWB (eds) Animal sonar: Processes and performance. Plenum Press, New York, pp 301–305
Henson OW Jr, Henson MM, Kobler JB, Pollak GD (1980) The constant frequency component of the biosonar signals of the bat Pteronotus parnellii parnellii. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum, New York, pp 913–916
Henson OW Jr, Pollak GD, Kobler JB, Henson MM, Goldman LJ (1982) Cochlear microphonic potentials elicited by biosonar signals in flying bats, Pteronotus p. parnellii. Hearing Res 7:127–147
Henson OW Jr, Schuller G, Vater M (1985) A comparative study of the physiological properties of the inner ear in Doppler shift compensating bats (Rhinolophus rouxi and Pteronotus parnellii). J Comp Physiol A 157:587–597
Henson OW Jr, Bishop AL, Keating AW, Kobler JB, Henson MM, Wilson BS, Hansen R (1987) Biosonar imaging of insects by Pteronotus p. parnellii, the mustached bat. Nat Geogr Res 3:82–101
Henson OW Jr, Keating AW, Huffman RF, Koplas P, Henson MM (1989) The effect of contralateral acoustic stimulation on the stability of cochlear resonance. Assoc Res Otolaryngol Abstr 12:339
Henson OW Jr, Koplas P, Keating AW, Huffman RF, Henson MM (1990) Cochlear resonance in the mustached bat: behavioral adaptations. Hearing Res 50:259–274
Huffman RF, Henson OW Jr (1991) Cochlear and CNS tonotopy: normal physiological shifts in the mustached bat. Hearing Res 56:79–85
Huffman RF, Henson OW Jr (1993) Labile cochlear tuning in the mustached bat. II. Concomitant shifts in neural tuning. J Comp Physiol A 171:735–748
Huffman RF, Keating AW, Henson OW Jr (1991) Mustached bats adjust biosonar emissions to accommodate shifts in cochlear resonance. Assoc Res Otolaryngol Abstr 14:23
Jen PH-S, Kamada T (1982) Analysis of orientation signals emitted by the CF-FM bat, Pteronotus p. parnellii and FM bat, Eptesicus fuscus during avoidance of moving and stationary obstacles. J Comp Physiol 148:389–398
Kim DO, Neely ST, Molnar CE, Matthews JW (1980) An active cochlear model with negative damping in the partition: comparison with Rhode's ante- and post-mortem observations. In: van den Brink G, Bilsen FW (eds) Psychophysical, physiological and behavioural studies in hearing. Delft University Press, Delft, pp 7–14
Kobler JB, Wilson BS, Henson OW Jr, Bishop AL (1985) Echo intensity compensation by echolocating bats. Hearing Res 20:99–108
Kössl M, Vater M (1985 a) Evoked acoustic emissions and cochlear microphonics in the mustache bat, Pteronotus parnellii. Hearing Res 19:157–170
Kössl M, Vater M (1985 b) The cochlear frequency map of the mustache bat, Pteronotus parnellii. J Comp Physiol A 157:687–697
Kössl M, Vater M (1990 a) Tonotopic organization of the cochlear nucleus of the mustache bat, Pteronotus parnellii. J Comp Physiol A 166:695–709
Kössl M, Vater M (1990 b) 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
LePage EL (1989) Functional role of the olivo-cochlear bundle: a motor unit control system in the mammalian cochlea. Hearing Res 38:177–198
Manley GA, Köppl C (1992) Effect of temperature on spontaneous emissions in the bobtail lizard. Assoc Res Otolaryngol Abstr 15:156
McNab BK (1969) The economics of temperature regulation in neotropical bats. Comp Biochem Physiol 31:227–268
Mott JB, Norton SJ, Neely ST, Warr WB (1989) Changes in spontaneous otoacoustic emissions produced by acoustic stimulation of the contralateral ear. Hearing Res 38:229–242
Neely ST, Kim DO (1983) An active cochlear model showing sharp tuning and high sensitivity. Hearing Res 9:123–130
Neely ST, Kim DO (1986) A model for active elements in cochlear biomechanics. J Acoust Soc Am 79:1472–1480
Novick A, Vaisnys JR (1964) Echolocation of flying insects by the bat Chilonycteris parnellii. Biol Bull 127:478–488
Ohyama K, Sato T, Wada H, Takasaka T (1992) Frequency instability of the spontaneous otoacoustic emissions in the guinea pig. Assoc Res Otolaryngol Abstr 15:150
Olsen JF, Suga N (1991) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding of relative velocity information. J Neurophysiol 65:1254–1274
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
Pollak GD, Casseday JH (1989) The neural basis of echolocation in bats. Springer, Berlin Heidelberg New York, pp 1–143
Pollak G, Henson OW Jr, Novick A (1972) Cochlear microphonic audiograms in the “pure tone” bat Chilonycteris parnellii parnellii. Science 176:66–68
Pollak G, Henson OW Jr, Johnson R (1979) Multiple specializations in the peripheral auditory system of the CF-FM bat, Pteronotus parnellii. J Comp Physiol 131:255–266
Probst R, Lonsbury-Martin BL, Martin GK (1991) A review of otoacoustic emissions. J Acoust Soc Am 89:2027–2067
Ross LS, Pollak GD (1989) Differential ascending projections to aural regions in the 60 kHz contour of the mustache bat's inferior colliculus. J Neurosci 9:2819–2834
Ross LS, Pollak GD, Zook JM (1988) Origin of ascending projections to an isofrequency region of the mustache bat's inferior colliculus. J Comp Neurol 270:488–505
Schnitzler H-U (1970 a) Echoortung bei der Fledermaus, Chilonycteris rubiginosa. Z Vergl Physiol 68:25–39
Schnitzler H-U (1970 b) Comparison of echolocation behavior in Rhinolophus ferrumequinum and Chilonycteris rubiginosa. Bidjr Dierk 40:77–80
Schuller G, Radtke-Schuller S (1988) Midbrain areas as candidates for audio-vocal interface in echolocating bats. In: Nachtigall PE, Moore PWB (eds) Animal sonar: Processes and performance. Plenum Press, New York, pp 93–98
Suga N, Jen PH-S (1976) Disproportionate tonotopic representation for processing CF-FM sonar signals in the mustache bat auditory cortex. Science 194:542–544
Suga N, Jen PH-S (1977) Further studies on the peripheral auditory system of the CF-FM bats specialized for fine frequency analysis of Doppler-shifted echoes. J Exp Biol 169:207–232
Suga N, Yajima Y (1988) Auditory-vocal integration in the midbrain of the mustached bat: periaqueductal gray and reticular formation. In: Newman JD (ed) The physiological control of mammalian vocalization. Plenum Press, New York, pp 87–107
Suga N, Simmons JA, Jen PH-S (1975) Peripheral specializations for fine analysis of Doppler-shifted echoes in the auditory system of the “CF-FM” bat Pteronotus parnellii. J Exp Biol 63:161–192
Suga N, Niwa H, Taniguchi I, Margoliash D (1987) The personalized auditory cortex of the mustached bat: adaptation for echolocation. J Neurophysiol 58:643–654
Thomas SP (1987) The physiology of bat flight. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 75–99
Thomas SP, Suthers RA (1972) The physiology and energetics of bat flight. J Exp Biol 57:317–335
Vater M (1987) Narrow-band frequency analysis in bats. In: Fenton MB, Racey P, Rayner JMV (eds) Recent advances in the study of bats. Cambridge University Press, Cambridge, pp 200–225
Vater M (1988) Cochlear physiology and anatomy in bats. In: Nachtigall PE, Moore PWB (eds) Animal sonar: Processes and performance. Plenum Press, New York, pp 225–241
Warr WB (1992) Organization of olivocochlear efferent systems in mammals. In: Fay RR, Popper AN, Webster DB (eds) Springer Series in Auditory Research, Vol I: The anatomy of mammalian auditory pathways. Springer, Berlin Heidelberg New York, in press
Wiederhold ML (1986) Physiology of the olivocochlear system. In: Altschuler RA, Bobbin RP, Hoffman DW (eds) Neurobiology of hearing: The cochlea. Raven Press, New York, pp 349–370
Wilson JP, Whitehead ML, Baker RJ (1986) The effect of temperature on otoacoustic emission tuning properties. In: Moore BCJ, Patterson RD (eds) Auditory frequency selectivity. Plenum, London, pp 39–46
Zook JM, Leake PA (1989) Connections and frequency representation in the auditory brainstem of the mustache bat, Pteronotus parnellii. J Comp Neurol 290:243–261
Zook JM, Winer JA, Pollak GD, Bodenhamer RD (1985) Topology of the central nucleus of the mustache bat's inferior colliculus: correlation of single unit properties and neuronal architecture. J Comp Neurol 231:530–546
Zwislocki JJ (1980) Theory of cochlear mechanics. Hearing Res 2:171–182
Zwislocki JJ, Kletsky EJ (1980) Micromechanics in the theory of cochlear mechanics. Hearing Res 2:505–512
Zwislocki JJ, Kletsky EJ (1982) What basilar-membrane tuning says about cochlear micromechanics. Am J Otolaryngol 3:4852
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Huffman, R.F., Henson, O.W. Labile cochlear tuning in the mustached bat. J Comp Physiol A 171, 725–734 (1993). https://doi.org/10.1007/BF00213069
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DOI: https://doi.org/10.1007/BF00213069