Abstract
This review is yet another attempt to explain how echolocation in bats or bat-like mammals came into existence. Attention is focused on neuronal specializations in the ascending auditory pathway of echolocating bats. Three different mechanisms are considered that may create a specific auditory sensitivity to echos: (1) time-windows of enhanced echo-processing opened by a corollary discharge of neuronal vocalization commands; (2) differentiation and expansion of ensembles of combination-sensitive neurons in the midbrain; and (3) corticofugal top-down modulations. The second part of the review interprets three different types of echolocation as adaptations to ecological niches, and presents the sophisticated cochlear specializations in constant-frequency/frequency-modulated bats as a case study of finely tuned differentiation. It is briefly discussed how a resonant mechanism in the inner ear of constant-frequency/frequency-modulated bats may have evolved in common mammalian cochlea.
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Abbreviations
- AVCN:
-
anteroventral cochlear nucleus
- CF:
-
constant frequency element of an echolocation signal
- DPOAE:
-
distortion product otoacoustic emission
- FM:
-
frequency-modulated echolocation signal
- IC:
-
inferior colliculus
- IHC:
-
inner hair cell
- INLL:
-
intermediate nucleus of the lateral lemniscus
- MSO:
-
medial superior olive
- OAE:
-
otoacoustic emission
- OHC:
-
outer hair cell
- PVCN:
-
posterior ventral cochlear nucleus
- SI:
-
sparsely innervated section of the cochlea
- SOC:
-
superior olivary complex
- VNLL:
-
ventral nucleus of the lateral lemniscus
References
Covey E, Casseday JH (1995) The lower brainstem auditory pathways. In: Popper AN, Fay RR (eds) Hearing in bats. Springer handbook of auditory research. Springer, Berlin Heidelberg New York, pp 235–295
Faulstich M, Kössl M (1997) Thalamonal alters cochlear mechanics in the mustached bat. Proc 20th Midwinter Res Meet Assoc Res Otolaryngol, p 11
Fitzpatrick DC, Kuwada S, Batra R, Trahiotis ( (1995) Neural responses to simple, simulated echoes in the auditory brainstem of the unanesthetized rabbit. J Neurophysiol 74:2469–2486
Gehr DD, Komiya H, Eggermont JJ (2000) Neuronal responses in cat primary auditory cortex to natural and altered species-specific sounds. Hear Res 150:27–42
Grinnell AD (1963) The neurophysiology of audition in bats: temporal parameters. J Physiol (Lond) 167:67–96
Grothe B, Neuweiler G (2000) The function of the medial superior olive in small mammals: temporal receptive fields in auditory analysis. J Comp Physiol A 186:413–423
Haplea S, Covey E, Casseday JH (1994) Frequency tuning and response latencies at three levels in the brainstem of the echolocating bat, Eptesicus fuscus. J Comp Physiol A 174:671–683
Henson MM, Henson OW (1991) Specializations for sharp tuning in the mustached bat: the tectorial membrane and the spiral limbus. Hear Res 35:237–258
Henson OW, 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
Kalko EKV, Schnitzler HU (1998) How echolocating bats approach and acquire food. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithonian Institution Press, Washington, DC, pp 197–204
Keller CH, Takahashi TT (1996) Response to simulated echoes by neurons in the barn owl's auditory space map. J Comp Physiol 178:499–512
Kössl M (1994) Evidence for a mechanical filter in the cochlea of the 'constant-frequency' bats, Rhinolophus rouxi and Pteronotus parnellii. Hear Res 72:73–80
Kössl M, Vater M (1985) The cochlear frequency map of the mustached bat, Pteronotus parnellii. J Comp Physiol A 157:687–697
Kössl M, Vater M (1989) Noradrenaline enhances temporal auditory contrast and neuronal timing in the cochlear nucleus of the mustached bat. J Neurosci 9:4169–4178
Kössl M, Vater M (1995) Cochlear structure and function in bats. In: Popper AN, Fay RR (eds) Hearing by bats. Springer, Berlin Heidelberg New York, pp 191–234
Kössl M, Vater M (1996a) Further studies on the mechanics of the cochlear partition in the mustached bat. II. A second cochlear frequency map derived from acoustic distortion products. Hear Res 94:78–86
Kössl M, Vater M (1996b) A tectorial membrane fovea in the cochlea of the mustached bat. Naturwissenschaften 83:89–91
Kössl M, Vater M (2000) Consequences of outer hair cell damage for otoacoustic emissions and audiovocal feedback in the mustached bat. J Assoc Res Otolaryngol 1:300–314
Kössl M, Mayer F, Frank G, Faulstich M, Russell IJ (1999) Evolutionary adaptations of cochlear function in Jamaican mormoopid bats. J Comp Physiol A 185:217–228
Link A, Marimuthu G, Neuweiler G (1986) Movement as a specific stimulus for prey catching behaviour in rhinolophid and hipposiderid bats. J Comp Physiol A 159:403–413
Litovsky RY (1998) Physiological studies on the precedence effect in the inferior colliculus of the kitten. J Acoust Soc Am 103:3139–3152
Litovsky RY, Yin TCT (1998) Physiological studies of the precedence effect in the inferior colliculus of the cat. I. Correlates of psychophysics. J Neurophysiol 80:1285–1301
Litovsky RY, Colburn HS, Yost WA, Guzman SJ (1999) The precedence effect. J Acoust Soc Am 106:1633–1653
Ma X, Suga N (2001) Corticofugal modulation of duration-tuned neurons in the midbrain auditory nucleus in bats. Proc Natl Acad Sci USA 98:14060–14065
Margoliash D, Fortune ES (1992) Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J Neurosci 12:4309–4326
Neuweiler G (1984) Foraging, echolocation and audition in bats. Naturwissenschaften 71:446–455
Neuweiler G (2000) Biology of bats. Oxford University Press, New York
Neuweiler G, Schmidt S (1993) Audition in echolocating bats. Curr Opin Neurobiol 3:563–569
Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behaviour and echolocation in the rufous horseshoe bat of Sri Lanka. Behav Ecol Sociobiol 20:53–67
Olsen JF, Suga N (1991) Combination-sensitive neurons in the medial geniculate body of the mustached bat: encoding target range information. J Neurophysiol 65:1275–1296
O'Neill WE, Suga N (1982) Encoding of target range and its representation in the auditory cortex of the mustached bat. J Neurosci 2:17–31
Padian K (1985) The origin and aerodynamics of flight in extinct vertebrates. Palaeontology 28:413–433
Portfors CV, Wenstrup JJ (1999) Delay tuned neurons in the inferior colliculus of the mustached bat: implications for analyses of target distance. J Neurophysiol 82:1326–1338
Portfors CV, Wenstrup JJ (2001) Responses to combinations of tones in the nuclei of the lateral lemniscus. JARO 2:104–117
Rauschecker JP, Tian B, Hauser M (1995) Processing of complex sounds in the macaque nonprimary auditory cortex. Science 268:111–114
Rayner JMV (1991) Complexity in a coupled system: flight, echolocation and evolution in bats. In: Schmidt-Kittler, Vogel K (eds) Constructional morphology and evolution. Springer, Berlin Heidelberg New York, pp 173–191
Roverud RC (1993) Neural computations for sound pattern recognition: evidence for summation of an array of frequency filters in an echolocating bat. J Neurosci 13:2306–2312
Roverud RC, Grinnell AD (1985) Echolocation sound features processed to provide distance information in the CF/FM bat, Noctilio albiventris: evidence for a gated time window utilizing both CF and FM components. J Comp Physiol A 156:457–469
Russell IJ, Kössl M (1999) Micromechanical responses to tones in the auditory fovea of the greater mustached bat's cochlea. J Neurophysiol 82:676–686
Schmidt S (1988) Evidence for a spectral basis of texture perception in bat sonar. Nature 331:617–619
Schnitzler HU, Kalko EKV (1998) How echolocating bats search and find food. In: Kunz TH, Racey PA (eds) Bat biology and conservation. Smithonian Institution Press, Washington, DC, pp 183–196
Schuller G (1979) Vocalization influences auditory processing in collicular neurons of the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol A 132:39–46
Schuller G, O'Neill WE, Radtke-Schuller S (1991) Facilitation and delay sensitivity of auditory cortex neurons in CF-FM bats, Rhinolophus rouxi and Pteronotus parnellii. Eur J Neurosci 3:1165–1181
Shera CA, Guinan JJ (1999) Evoked otoacoustic emissions arise by two fundamentally different mechanisms: a taxonomy for mammalian OAEs. J Acoust Soc Am 105:782–798
Simmons JA, Stein RA (1980) Acoustic imaging in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol A 135:61–84
Yan J, Suga N (1996) Corticofugal modulation of time-domain processing of biosonar information in bats. Science 273:1100–1103
Yost WA, Guzman SJ (1996) Auditory processing of sound sources: Is there an echo in here? Curr Direct Psychol Sci 5:125–131
Acknowledgements
I thank Prof. Manfred Kössl, Frankfurt for critically reading the manuscript, and S. Peisker for preparing the figures. I am also grateful to an anonymous reviewer who helped to clarify the text.
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Neuweiler, G. Evolutionary aspects of bat echolocation. J Comp Physiol A 189, 245–256 (2003). https://doi.org/10.1007/s00359-003-0406-2
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DOI: https://doi.org/10.1007/s00359-003-0406-2