The adaptive value of increasing pulse repetition rate during hunting by echolocating bats

Philip H.-S. JEN

PDF(525 KB)
PDF(525 KB)
Front. Biol. ›› 2013, Vol. 8 ›› Issue (2) : 198-215. DOI: 10.1007/s11515-012-1212-4
REVIEW
REVIEW

The adaptive value of increasing pulse repetition rate during hunting by echolocating bats

Author information +
History +

Abstract

During hunting, bats of suborder Microchiropetra emit intense ultrasonic pulses and analyze the weak returning echoes with their highly developed auditory system to extract the information about insects or obstacles. These bats progressively shorten the duration, lower the frequency, decrease the intensity and increase the repetition rate of emitted pulses as they search, approach, and finally intercept insects or negotiate obstacles. This dynamic variation in multiple parameters of emitted pulses predicts that analysis of an echo parameter by the bat would be inevitably affected by other co-varying echo parameters. The progressive increase in the pulse repetition rate throughout the entire course of hunting would presumably enable the bat to extract maximal information from the increasing number of echoes about the rapid changes in the target or obstacle position for successful hunting. However, the increase in pulse repetition rate may make it difficult to produce intense short pulse at high repetition rate at the end of long-held breath. The increase in pulse repetition rate may also make it difficult to produce high frequency pulse due to the inability of the bat laryngeal muscles to reach its full extent of each contraction and relaxation cycle at a high repetition rate. In addition, the increase in pulse repetition rate increases the minimum threshold (i.e. decrease auditory sensitivity) and the response latency of auditory neurons. In spite of these seemingly physiological disadvantages in pulse emission and auditory sensitivity, these bats do progressively increase pulse repetition rate throughout a target approaching sequence. Then, what is the adaptive value of increasing pulse repetition rate during echolocation? What are the underlying mechanisms for obtaining maximal information about the target features during increasing pulse repetition rate? This article reviews the electrophysiological studies of the effect of pulse repetition rate on multiple-parametric selectivity of neurons in the central nucleus of the inferior colliculus of the big brown bat, Eptesicus fuscus using single repetitive sound pulses and temporally patterned trains of sound pulses. These studies show that increasing pulse repetition rate improves multiple-parametric selectivity of inferior collicular neurons. Conceivably, this improvement of multiple-parametric selectivity of collicular neurons with increasing pulse repetition rate may serve as the underlying mechanisms for obtaining maximal information about the prey features for successful hunting by bats.

Keywords

bat / echolocation / inferior colliculus / multiple-parametric selectivity / pulse repetition rate

Cite this article

Download citation ▾
Philip H.-S. JEN. The adaptive value of increasing pulse repetition rate during hunting by echolocating bats. Front Biol, 2013, 8(2): 198‒215 https://doi.org/10.1007/s11515-012-1212-4

References

[1]
Bormann J (1988). Electrophysiology of GABAA and GABAB receptor subtypes. Trends Neurosci, 11(3): 112–116
CrossRef Pubmed Google scholar
[2]
Bormann J (2000). The ‘ABC’ of GABA receptors. Trends Pharmacol Sci, 21(1): 16–19
CrossRef Pubmed Google scholar
[3]
Brand A, Urban R, Grothe B (2000). Duration tuning in the mouse auditory midbrain. J Neurophysiol, 84(4): 1790–1799
Pubmed
[4]
Brosch M, Schreiner C E (1997). Time course of forward masking tuning curves in cat primary auditory cortex. J Neurophysiol, 77(2): 923–943
Pubmed
[5]
Calford M B, Semple M N (1995). Monaural inhibition in cat auditory cortex. J Neurophysiol, 73(5): 1876–1891
Pubmed
[6]
Casseday J H, Covey E (1995). Mechanisms for analysis of auditory temporal patterns in the brainstem of echolocating bats. In: Covey E, Hawkins HL, Port RF (eds). Neural representation of temporal patterns. Plenum, New York, pp 25–51
[7]
Casseday J H, Ehrlich D, Covey E (1994). Neural tuning for sound duration: role of inhibitory mechanisms in the inferior colliculus. Science, 264(5160): 847–850
CrossRef Pubmed Google scholar
[8]
Casseday J H, Ehrlich D, Covey E (2000). Neural measurement of sound duration: control by excitatory-inhibitory interactions in the inferior colliculus. J Neurophysiol, 84(3): 1475–1487
Pubmed
[9]
Chen G D (1998). Effects of stimulus duration on responses of neurons in the chinchilla inferior colliculus. Hear Res, 122(1-2): 142–150
CrossRef Pubmed Google scholar
[10]
Chen Q C, Jen P H S (1994). Pulse repetition rate increases the minimum threshold and latency of auditory neurons. Brain Res, 654(1): 155–158
CrossRef Pubmed Google scholar
[11]
Condon C J, White K R, Feng A S (1994). Processing of amplitude-modulated signals that mimic echoes from fluttering targets in the inferior colliculus of the little brown bat, Myotis lucifugus. J Neurophysiol, 71(2): 768–784
Pubmed
[12]
Cooper J R, Bloom F E, Roth R H (1982). The Biomedical Basis of Neuropharmacology, New York: Oxford University Press
[13]
Covey E, Casseday J H (1995). The lower brainstem auditory pathways. In: Popper A N, Fay R R (Eds.), Springer handbook of Auditory Research V5 Hearing by Bats. New York: Springer, pp 235–295
[14]
Covey E, Casseday J H (1999). Timing in the auditory system of the bat. Annu Rev Physiol, 61(1): 457–476
CrossRef Pubmed Google scholar
[15]
de Ribaupierre F, Goldstein M H Jr, Yeni-Komshian G (1972). Cortical coding of repetitive acoustic pulses. Brain Res, 48: 205–225
CrossRef Pubmed Google scholar
[16]
Ehrlich D, Casseday J H, Covey E (1997). Neural tuning to sound duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Neurophysiol, 77(5): 2360–2372
Pubmed
[17]
Faingold C L, Boersma Anderson C A, Caspary D M (1991). Involvement of GABA in acoustically-evoked inhibition in inferior colliculus neurons. Hear Res, 52(1): 201–216
CrossRef Pubmed Google scholar
[18]
Faure P A, Fremouw T, Casseday J H, Covey E (2003). Temporal masking reveals properties of sound-evoked inhibition in duration-tuned neurons of the inferior colliculus. J Neurosci, 23(7): 3052–3065
Pubmed
[19]
Feng A S, Condon C J, White K R (1994). Stroboscopic hearing as a mechanism for prey discrimination in frequency-modulated bats? J Acoust Soc Am, 95(5): 2736–2744
CrossRef Pubmed Google scholar
[20]
Feng A S, Hall J C, Gooler D M (1990). Neural basis of sound pattern recognition in anurans. Prog Neurobiol, 34(4): 313–329
CrossRef Pubmed Google scholar
[21]
Freyman R L, Clifton R K, Litovsky R Y (1991). Dynamic processes in the precedence effect. J Acoust Soc Am, 90(2): 874–884
CrossRef Pubmed Google scholar
[22]
Fubara B M, Casseday J H, Covey E, Schwartz-Bloom R D (1996). Distribution of GABAA, GABAB, and glycine receptors in the central auditory system of the big brown bat, Eptesicus fuscus. J Comp Neurol, 369(1): 83–92
CrossRef Pubmed Google scholar
[23]
Fuzessery Z M, Hall J C (1996). Role of GABA in shaping frequency tuning and creating FM sweep selectivity in the inferior colliculus. J Neurophysiol, 76(2): 1059–1073
Pubmed
[24]
Fuzessery Z M, Hall J C (1999). Sound duration selectivity in the pallid bat inferior colliculus. Hear Res, 137(1-2): 137–154
CrossRef Pubmed Google scholar
[25]
Fuzessery Z M, Pollak G D (1985). Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study. J Neurophysiol, 54(4): 757–781
Pubmed
[26]
Galarreta M, Hestrin S (1998). Frequency-dependent synaptic depression and the balance of excitation and inhibition in the neocortex. Nat Neurosci, 1(7): 587–594
CrossRef Pubmed Google scholar
[27]
Galazyuk A V, Feng A S (1997). Encoding of sound duration by neurons in the auditory cortex of the little brown bat, Myotis lucifugus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 180(4): 301–311
CrossRef Pubmed Google scholar
[28]
Galazyuk A V, Llano D, Feng A S (2000). Temporal dynamics of acoustic stimuli enhance amplitude tuning of inferior colliculus neurons. J Neurophysiol, 83(1): 128–138
Pubmed
[29]
Glendenning K K, Baker B N, Hutson K A, Masterton R B (1992). Acoustic chiasm V: inhibition and excitation in the ipsilateral and contralateral projections of LSO. J Comp Neurol, 319(1): 100–122
CrossRef Pubmed Google scholar
[30]
Gooler D M, Feng A S (1992). Temporal coding in the frog auditory midbrain: the influence of duration and rise-fall time on the processing of complex amplitude-modulated stimuli. J Neurophysiol, 67(1): 1–22
Pubmed
[31]
Griffin D R (1958) Listening in the Dark. Yale University Press, New Haven, CT (reprinted by Comstock, Ithaca, 1986
[32]
Grinnell A D (1963). The neurophysiology of audition in bats: directional localization and binaural. J Physiol, (Lond) 167: 97–113
[33]
Grinnell A D, Grinnell V S (1965). Neural correlates of vertical localization by echolocating bats. J Physiol, (Lond) 181:830–851
[34]
Grothe B, Covey E, Casseday J H (1996). Spatial tuning of neurons in the inferior colliculus of the big brown bat: effects of sound level, stimulus type and multiple sound sources. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 179(1): 89–102
CrossRef Pubmed Google scholar
[35]
Harnischfeger G, Neuweiler G, Schlegel P (1985). Interaural time and intensity coding in superior olivary complex and inferior colliculus of the echolocating bat Molossus ater. J Neurophysiol, 53(1): 89–109
Pubmed
[36]
Hartley D J (1992a). Stabilization of perceived echo amplitudes in echolocating bats. I. Echo detection and automatic gain control in the big brown bat, Eptesicus fuscus, and the fishing bat, Noctilio leporinus. J Acoust Soc Am, 91(2): 1120–1132
CrossRef Pubmed Google scholar
[37]
Hartley D J (1992b). Stabilization of perceived echo amplitudes in echolocating bats. II. The acoustic behavior of the big brown bat, Eptesicus fuscus, when tracking moving prey. J Acoust Soc Am, 91(2): 1133–1149
CrossRef Pubmed Google scholar
[38]
He J F, Hashikawa T, Ojima H, Kinouchi Y (1997). Temporal integration and duration tuning in the dorsal zone of cat auditory cortex. J Neurosci, 17(7): 2615–2625
Pubmed
[39]
Henson O W Jr (1965). The Activity and Function of the Middle Ear Muscles in Eecholocating Bats. J Physiol, (London) 180: 871–887
[40]
Henson O W Jr (1970). The ear and audition. In: Biology of bats, Vol. II (ed. W.A. Wimsatt),pp. 181–264. New York: Academic Press
[41]
Hiryu S, Hagino T, Riquimaroux H, Watanabe Y (2007). Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. J Acoust Soc Am, 121(3): 1749–1757
CrossRef Pubmed Google scholar
[42]
Hocherman S, Gilat E (1981). Dependence of auditory cortex evoked unit activity on interstimulus interval in the cat. J Neurophysiol, 45(6): 987–997
Pubmed
[43]
Hou T T, Wu M, Jen P H S (1992). Pulse repetition rate and duration affect the responses of bat auditory cortical neurons. Chin J Physiol, 35(4): 259–278
Pubmed
[44]
Jen P H S (1980). Coding of directional information by single neurones in the S-segment of the FM bat, Myotis lucifugus. J Exp Biol, 87: 203–216
Pubmed
[45]
Jen P H S, Chen Q C (1998). The effect of pulse repetition rate, pulse intensity, and bicuculline on the minimum threshold and latency of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 182(4): 455–465
CrossRef Pubmed Google scholar
[46]
Jen P H S, Feng R, Chen B (2003). GABAergic inhibition and the effect of sound direction on rate-intensity functions of inferior collicular neurons of the big brown Bat, Eptesicus fuscus. Chin J Physiol, 46(2): 83–90
Pubmed
[47]
Jen P H S, Feng R B (1999). Bicuculline application affects discharge pattern and pulse-duration tuning characteristics of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 184(2): 185–194
CrossRef Pubmed Google scholar
[48]
Jen P H S, Hou T T, Wu M (1993). Neurons in the inferior colliculus, auditory cortex and pontine nuclei of the FM bat, Eptesicus fucus respond to pulse repetition rate differently. Brain Res, 613(1): 152–155
CrossRef Pubmed Google scholar
[49]
Jen P H S, Kamada T (1982). Analysis of orientation signals emitted by the CF-FM bat, Pteronotus parnellii parnellii and the FM bat, Eptesicus fuscus during avoidance of moving and stationary obstacles. J Comp Physiol, 148(3): 389–398
CrossRef Google scholar
[50]
Jen P H S, Ostwald J, Suga N (1978). Electrophysiological properties of the acoustic middle ear and laryngeal muscles reflexes in the awake echolocating FM bats, Myotis lucifugus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 124(1): 61–73
CrossRef Google scholar
[51]
Jen P H S, Schlegel P (1982). Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol, 147(3): 351–363
CrossRef Google scholar
[52]
Jen P H S, Suga N (1976). Coordinated activities of middle-ear and laryngeal muscles in echolocating bats. Science, 191(4230): 950–952
CrossRef Pubmed Google scholar
[53]
Jen P H S, Sun X D (1984). Pinna orientation determines the maximal directional sensitivity of bat auditory neurons. Brain Res, 301(1): 157–161
CrossRef Pubmed Google scholar
[54]
Jen P H S, Sun X D, Chen D M, Teng H B (1987). Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus. Brain Res, 419(1-2): 7–18
CrossRef Pubmed Google scholar
[55]
Jen P H S, Sun X D, Lin P J (1989). Frequency and space representation in the primary auditory cortex of the FM bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 165: 1–14
CrossRef Google scholar
[56]
Jen P H S, Wu C H (2005). The role of GABAergic inhibition in shaping the response size and duration selectivity of bat inferior collicular neurons to sound pulses in rapid sequences. Hear Res, 202(1-2): 222–234
CrossRef Pubmed Google scholar
[57]
Jen P H S, Wu C H, Luan R H, Zhou X M (2002). GABAergic inhibition contributes to pulse repetition rate-dependent frequency selectivity in the inferior colliculus of the big brown bat, Eptesicus fuscus. Brain Res, 948(1-2): 159–164
CrossRef Pubmed Google scholar
[58]
Jen P H S, Wu M (1993). Directional sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, to sounds delivered from selected horizontal and vertical angles. Chin J Physiol, 36(1): 7–18
Pubmed
[59]
Jen P H S, Zhang J (2000). The role of GABAergic inhibition on direction-dependent sharpening of frequency tuning in bat inferior collicular neurons. Brain Res, 862(1-2): 127–137
CrossRef Pubmed Google scholar
[60]
Jen P H S, Zhou X M (1999). Temporally patterned pulse trains affect duration tuning characteristics of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 185(5): 471–478
CrossRef Pubmed Google scholar
[61]
Jen P H S, Zhou X M, Wu C H (2001). Temporally patterned pulse trains affect frequency tuning and intensity coding of inferior collicular neurons of the big brown bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 187: 605–616
CrossRef Google scholar
[62]
Kick S A, Simmons J A (1984). Automatic gain control in the bat’s sonar receiver and the neuroethology of echolocation. J Neurosci, 4(11): 2725–2737
Pubmed
[63]
Klug A, Park T J, Pollak G D (1995). Glycine and GABA influence binaural processing in the inferior colliculus of the mustache bat. J Neurophysiol, 74(4): 1701–1713
Pubmed
[64]
Kobler J B, Wilson B S, Henson O W Jr, Bishop A L (1985). Echo intensity compensation by echolocating bats. Hear Res, 20(2): 99–108
CrossRef Pubmed Google scholar
[65]
Koch U, Grothe B (1998). GABAergic and glycinergic inhibition sharpens tuning for frequency modulations in the inferior colliculus of the big brown bat. J Neurophysiol, 80(1): 71–82
Pubmed
[66]
Lawrence B D, Simmons J A (1982). Echolocation in bats: the external ear and perception of the vertical positions of targets. Science, 218(4571): 481–483
CrossRef Pubmed Google scholar
[67]
Le Beau F E, Rees A, Malmierca M S (1996). Contribution of GABA- and glycine-mediated inhibition to the monaural temporal response properties of neurons in the inferior colliculus. J Neurophysiol, 75(2): 902–919
Pubmed
[68]
LeBeau F E, Malmierca M S, Rees A (2001). Iontophoresis in vivo demonstrates a key role for GABA(A) and glycinergic inhibition in shaping frequency response areas in the inferior colliculus of guinea pig. J Neurosci, 21(18): 7303–7312
Pubmed
[69]
Litovsky R Y, Yin T C (1998). Physiological studies of the precedence effect in the inferior colliculus of the cat. II. Neural mechanisms. J Neurophysiol, 80(3): 1302–1316
Pubmed
[70]
Lu Y, Jen P H S (2001). GABAergic and glycinergic neural inhibition in excitatory frequency tuning of bat inferior collicular neurons. Exp Brain Res, 141(3): 331–339
CrossRef Pubmed Google scholar
[71]
Lu Y, Jen P H S (2002). Interaction of excitation and inhibition in inferior collicular neurons of the big brown bat, Eptesicus fuscus. Hear Res, 169(1-2): 140–150
CrossRef Pubmed Google scholar
[72]
Lu Y, Jen P H S, Wu M (1998). GABAergic disinhibition affects responses of bat inferior collicular neurons to temporally patterned sound pulses. J Neurophysiol, 79(5): 2303–2315
Pubmed
[73]
Lu Y, Jen P H S, Zheng Q Y (1997). GABAergic disinhibition changes the recovery cycle of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 181(4): 331–341
CrossRef Pubmed Google scholar
[74]
Malmierca M S, Leergaard T B, Bajo V M, Bjaalie J G, Merchan M A (1998). Anatomic evidence of a 3-D mosaic pattern of tonotopic organization in the ventral complex of the lateral lemniscus in cat. J Neurosci, 18: 10603–10618
Pubmed
[75]
Masters W M, Moffat A J M, Simmons J A (1985). Sonar tracking of horizontally moving targets by the big brown bat Eptesicus fuscus. Science, 228(4705): 1331–1333
CrossRef Pubmed Google scholar
[76]
McAlpine D, Palmer A R (2002). Blocking GABAergic inhibition increases sensitivity to sound motion cues in the inferior colliculus. J Neurosci, 22(4): 1443–1453
Pubmed
[77]
Moriyama T, Hou T T, Wu M, Jen P H S (1994). Responses of inferior collicular neurons of the FM bat, Eptesicus fuscus, to pulse trains with varied pulse amplitudes. Hear Res, 79(1–2): 105–114
CrossRef Pubmed Google scholar
[78]
Moriyama T, Wu M I, Jen P H S (1997). Responses of bat inferior collicular neurons to recorded echolocation pulse trains. Chin J Physiol, 40(1): 9–17
Pubmed
[79]
Narins P M, Capranica R R (1980). Neural adaptation for processing the two-tone call of the Puerto Rican tree frog, Eleuthereodactylus coqui. Brain Behav Evol, 18(1): 48–66
CrossRef Google scholar
[80]
Novick A (1971). Echolocation in bats: some aspects of pulse design. Am Sci, 59(2): 198–209
Pubmed
[81]
Novick A, Griffin D R (1961). Laryngeal mechanisms in bats for the production of orientation sounds. J Exp Zool, 148(2): 125–145
CrossRef Pubmed Google scholar
[82]
Oliver D L, Shneiderman A (1991). The anatomy of the inferior colliculus: a cellular basis for integration of monaural and binaural information. In: Altschuler R A, Bobbin R P, Clopton B M, Hoffmann D W (Eds), Neurobiology of Hearing pp195–222, New York: Raven
[83]
Oliver D L, Winer J A, Beckius G E, Saint Marie R L (1994). Morphology of GABAergic neurons in the inferior colliculus of the cat. J Comp Neurol, 340(1): 27–42
CrossRef Pubmed Google scholar
[84]
Park T J, Pollak G D (1993). GABA shapes sensitivity to interaural intensity disparities in the mustache bat’s inferior colliculus: implications for encoding sound location. J Neurosci, 13(5): 2050–2067
Pubmed
[85]
Park T J, Pollak G D (1994). Azimuthal receptive fields are shaped by GABAergic inhibition in the inferior colliculus of the mustache bat. J Neurophysiol, 72(3): 1080–1102
Pubmed
[86]
Pérez-González D, Malmierca M S, Moore J M, Hernández O, Covey E (2006). Duration selective neurons in the inferior colliculus of the rat: topographic distribution and relation of duration sensitivity to other response properties. J Neurophysiol, 95(2): 823–836
CrossRef Pubmed Google scholar
[87]
Perkins K L, Wong R K (1997). The depolarizing GABA response. Can J Physiol Pharmacol, 75(5): 516–519
CrossRef Pubmed Google scholar
[88]
Phillips D P, Hall S E, Hollett J L (1989). Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. J Acoust Soc Am, 85(6): 2537–2549
CrossRef Pubmed Google scholar
[89]
Pinheiro A D, Wu M, Jen P H S (1991). Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 169(1): 69–85
CrossRef Pubmed Google scholar
[90]
Popper A N, Fay R R (1995). Hearing by bats. New York: Springer
[91]
Rabow L E, Russek S J, Farb D H (1995). From ion currents to genomic analysis: recent advances in GABA-R research. Synapse, 21(3): 174–189
CrossRef Google scholar
[92]
Roberts R C, Ribak C E (1987a). An electron microscopic study of GABAergic neurons and terminals in the central nucleus of the inferior colliculus of the rat. J Neurocytol, 16(3): 333–345
CrossRef Pubmed Google scholar
[93]
Roberts R C, Ribak C E (1987b). GABAergic neurons and axon terminals in the brainstem auditory nuclei of the gerbil. J Comp Neurol, 258(2): 267–280
CrossRef Pubmed Google scholar
[94]
Roverud R C (1989). A gating mechanism for sound pattern recognition is correlated with the temporal structure of echolocation sound in the rufous horseshoe bat. J Comp Physiol, 166(2): 243–249
CrossRef Google scholar
[95]
Roverud R C, Grinnell A D (1985). Discrimination performance and echolocation signal integration requirements for target detection and distance discrimination in the CF/FM bat, Noctilio albiventris. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 156(4): 447–456
CrossRef Google scholar
[96]
Saint Marie R L, Morest D K, Brandon C J (1989). The form and distribution of GABAergic synapses on the principal cell types of the ventral cochlear nucleus of the cat. Hear Res, 42(1): 97–112
CrossRef Pubmed Google scholar
[97]
Schlegel P A (1977). Directional coding by binaural brainstem units of the CF-FM bat Rhinolophus ferrumequinum. J Comp Physiol, 118(3): 327–352
CrossRef Google scholar
[98]
Schlegel P A, Jen P H S, Singh S (1988). Auditory spatial sensitivity of inferior collicular neurons of echolocating bats. Brain Res, 456(1): 127–138
CrossRef Pubmed Google scholar
[99]
Schnitzler H U, Grinnell A D (1977). Directional sensitivity of echolocation in the horseshoe bat Rhinolophus ferrumequinum I. Directionality of sound emission. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 116(1): 51–61
CrossRef Google scholar
[100]
Schnitzler H U, Henson O W (1980). Performance of airborne animal sonar systems. I. Microchiroptera. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum Press, New York,pp 109–182
[101]
Shannon R V, Zeng F G, Kamath V, Wygonski J, Ekelid M (1995). Speech recognition with primary temporal cues. Science (USA), 270: 303–304
[102]
Shimozawa T, Suga N, Hendler P, Schuetze S (1974). Directional sensitivity of echolocation system in bats producing frequency-modulated signals. J Exp Biol, 60(1): 53–69
Pubmed
[103]
Simmons J A, Fenton M B, O’Farrell M J (1979). Echolocation and pursuit of prey by bats. Science, 203(4375): 16–21
CrossRef Pubmed Google scholar
[104]
Simmons J A, Kick S A, Lawrence B D, Hale C, Bard C, Escudie B (1983). Acuity of horizontal angle discrimination by the echolocatingbat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 153: 321–330
CrossRef Google scholar
[105]
Simmons J A, Moffat A J, Masters W M (1992). Sonar gain control and echo detection thresholds in the echolocating bat, Eptesicus fuscus. J Acoust Soc Am, 91(2): 1150–1163
CrossRef Pubmed Google scholar
[106]
Smalling J M, Galazyuk A V, Feng A S (2001). Stimulation rate influences frequency tuning characteristics of inferior colliculus neurons in the little brown bat, Myotis lucifugus. Neuroreport, 12(16): 3539–3542
CrossRef Pubmed Google scholar
[107]
Smotherman M, Metzner W (2003). Effects of echo intensity on Doppler-shift compensation behavior in horseshoe bats. J Neurophysiol, 89(2): 814–821
CrossRef Pubmed Google scholar
[108]
Suga N (1964) Single unit activity in cochlear nucleus and inferior colliculus of echolocating bats. J Physiol, (Lond) 172:449–474
[109]
Suga N (1997) Parallel-hierarchical processing of complex sounds for specialized auditory function. In: Crocker MJ (Ed) Encyclopedia of Acoustics, New York, John Wiley & Sons, Inc. pp 1409–1418
[110]
Suga N, Jen P H S (1975). Peripheral control of acoustic signals in the auditory system of echolocating bats. J Exp Biol, 62(2): 277–311
Pubmed
[111]
Suga N, Schlegel P (1972). Neural attenuation of responses to emitted sounds in echolocating bat. Science (USA), 177: 82–84
[112]
Suga N, Shimozawa T (1974). Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science, 183(130): 1211–1213 (USA)
CrossRef Pubmed Google scholar
[113]
Suga N, Yan J, Zhang Y F (1998) The processing of species-specific complex sounds by the ascending and descending auditory systems. In Poon P, Bruggie J (Eds), Central Auditory Processing and Neural Modeling. New York: Plenum Press, pp 55–70
[114]
Sun X D, Jen P H S (1987). Pinna position affects the auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus. Hear Res, 27(3): 207–219
CrossRef Pubmed Google scholar
[115]
Surlykke A, Moss C F (2000). Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J Acoust Soc Am, 108(5): 2419–2429
CrossRef Pubmed Google scholar
[116]
Vater M, Habbicht H, Kössl M, Grothe B (1992). The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 171(4): 541–553
CrossRef Pubmed Google scholar
[117]
Wallach H, Newman E B, Rosenzweig M R (1949). The precedence effect in sound localization. Am J Psychol, 62(3): 315–336
CrossRef Pubmed Google scholar
[118]
Wu C H, Jen P H S (2006a). GABA-mediated echo duration selectivity of inferior collicular neurons of Eptesicus fuscus, determined with single pulses and pulse-echo pairs. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 192(9): 985–1002
CrossRef Pubmed Google scholar
[119]
Wu C H, Jen P H S (2006b). The role of GABAergic inhibition in shaping duration selectivity of bat inferior collicular neurons determined with temporally patterned sound trains. Hear Res, 215(1–2): 56–66
CrossRef Pubmed Google scholar
[120]
Wu C H, Jen P H S (2008). Echo frequency selectivity of duration-tuned inferior collicular neurons of the big brown bat, Eptesicus fuscus, determined with pulse-echo pairs. Neuroscience, 156(4): 1028–1038
CrossRef Pubmed Google scholar
[121]
Wu L G, Betz W J (1998). Kinetics of synaptic depression and vesicle recycling after tetanic stimulation of frog motor nerve terminals. Biophys J, 74(6): 3003–3009
CrossRef Pubmed Google scholar
[122]
Wu M, Hou E T T, Jen P H S (1996). Responses of bat inferior collicular and auditory cortical neurons to pulsatile amplitude modulated sound pulses. Chin J Physiol, 39(3): 1–7
Pubmed
[123]
Wu M, Jen P H S (1991). Encoding of acoustic stimulus intensity by inferior collicular neurons of the big brown bat, Eptesicus fuscus. Chin J Physiol, 34: 145–155
[124]
Wu M, Jen P H S (1995b). Directional sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus, determined with temporally varied sound pulses. Le Rhinolophe, 11: 75–81
[125]
Wu M, Jen P H S (1996). Temporally patterned sound pulses affect directional sensitivity of inferior collicular neurons of the big brown bat, Eptesicus fuscus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 179(3): 385–393
CrossRef Google scholar
[126]
Wu M I, Jen P H S (1995a). Responses of pontine neurons of the big brown bat, Eptesicus fuscus, to temporally patterned sound pulses. Hear Res, 85(1-2): 155–168
CrossRef Pubmed Google scholar
[127]
Yang L, Pollak G D, Resler C (1992). GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J Neurophysiol, 68(5): 1760–1774
Pubmed
[128]
Yost W A, Guzman S J (1996). Auditory processing of sound sources: Is there an echo in here? Curr Dir Psychol Sci, 5(4): 125–131
CrossRef Google scholar
[129]
Yost W A, Soderquist D R (1984). The precedence effect: revisited. J Acoust Soc Am, 76(5): 1377–1383
CrossRef Pubmed Google scholar
[130]
Zhang H, Xu J, Feng A S (1999). Effects of GABA-mediated inhibition on direction-dependent frequency tuning in the frog inferior colliculus. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 184(1): 85–98
CrossRef Pubmed Google scholar
[131]
Zhou X M, Jen P H S (2000). Neural inhibition sharpens auditory spatial sensitivity of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 186(4): 389–398
CrossRef Google scholar
[132]
Zhou X M, Jen P H S (2001). The effect of sound intensity on duration-tuning characteristics of bat inferior collicular neurons. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 187(1): 63–73
CrossRef Pubmed Google scholar
[133]
Zhou X M, Jen P H S (2002a). The effect of sound duration on rate-amplitude functions of inferior collicular neurons in the big brown bat, Eptesicus fuscus. Hear Res, 166(1-2): 124–135
CrossRef Pubmed Google scholar
[134]
Zhou X M, Jen P H S (2002b). The role of GABAergic inhibition in shaping directional selectivity of bat inferior collicular neurons determined with temporally patterned pulse trains. J Comp Physiol A Neuroethol Sens Neural Behav Physiol, 188(10): 815–826
CrossRef Pubmed Google scholar
[135]
Zhou X M, Jen P H S (2003). The effect of bicuculline application on azimuth-dependent recovery cycle of inferior collicular neurons of the big brown bat, Eptesicus fuscus. Brain Res, 973(1): 131–141
CrossRef Pubmed Google scholar
[136]
Zhou X M, Jen P H S (2004). Azimuth-dependent recovery cycle affects directional selectivity of bat inferior collicular neurons determined with sound pulses within a pulse train. Brain Res, 1019(1–2): 281–288
CrossRef Pubmed Google scholar
[137]
Zhou X M, Jen P H S (2006). Duration selectivity of bat inferior collicular neurons improves with increasing pulse repetition rate. Chin J Physiol, 49(1): 46–55
Pubmed
[138]
Zucker R S (1989). Short-term synaptic plasticity. Annu Rev Neurosci, 12(1): 13–31
CrossRef Pubmed Google scholar
[139]
Zurek P M (1980). The precedence effect and its possible role in the avoidance of interaural ambiguities. J Acoust Soc Am, 67(3): 953–964
CrossRef Pubmed Google scholar

Acknowledgments

The research works described in this review article have been supported by the National Science Foundation and National Institute of Health of USA, Human Frontier Science Program of International Brain Research Organization, the Research Board, Research Council, College of Arts and Sciences, and Division of Biologic Sciences of University of Missouri-Columbia, USA. I particularly like to express my sincere thanks to my former coworkers in participation of all the studies described in this review. They are Drs, Qi-Cai Chen, Rui-Ben Feng, Tsutomu Kamada, Erika Hou, Ruihong Luan, Toshio Moriyama, Danial Pinheiro, Peter Schlegel, Xinde Sun, Haibing Teng, Min Wu, Chung Hsin Wu, Ji Ping Zhang and Xiaoming Zhou.

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg
PDF(525 KB)

Accesses

Citations

Detail

Sections
Recommended

/