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Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus

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Summary

  1. 1.

    Encoding of temporal stimulus parameters by inferior collicular (IC) neurons of Eptesicus fuscus was studied by recording their responses to a wide range of repetition rates (RRs) and durations at several stimulus intensities under free field stimulus conditions.

  2. 2.

    The response properties of 424 IC neurons recorded were similar to those reported in previous studies of this species.

  3. 3.

    IC neurons were classified as low-pass, band-pass, and high-pass according to their preference for RRs (Fig. 6) and/or durations (Fig. 8) characteristic of, respectively, search, approach, or terminal phases of echolocation. These neurons selectively process stimuli characteristic of the various phases of hunting.

  4. 4.

    Best RRs (Fig. 7A) and best durations (Fig. 7B) were not correlated with either the BFs or recording depths (Figs. 7C, D and 10). This suggests that each isofrequency lamina is capable of processing RRs and durations of all hunting phases.

  5. 5.

    Responses of one half of IC neurons studied were correlated with the stimulus duty cycle (Fig. 9). These neurons may preferentially process terminal phase information when the bat's pulse emission duty cycle increases.

  6. 6.

    While the stimulus RR affected the dynamic range and overall profile of the intensity rate function (Fig. 11), only little effect was observed with different stimulus durations (Fig. 12).

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Abbreviations

BF :

best frequency

IC :

inferior colliculus

MT :

minimum threshold

PAM :

pulsatile amplitude modulation

RR :

repetition rate

SAM :

sinusoidal amplitude modulation

References

  • Bliss TVP, Lomo T (1973) Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J Physiol (Lond) 232:331–356

    Google Scholar 

  • Brenowitz EA, Rose G, Capranica RR (1985) Neural correlates of temperature coupling in the vocal communication system of the gray treefrog (Hyla versicolor). Brain Res 359:364–367

    Google Scholar 

  • Busnel RG (ed) (1967) Animal sonar systems — biology and bionics, INRA-CNRZ, Jouy-en-Josas 78, France

  • Busnel RG, Fish JF (eds) (1980) Animal sonar systems. Plenum Press, New York

    Google Scholar 

  • Cahlander DA, McCue JJG, Webster FA (1964) The determination of distance by echolocating bats. Nature 201:544–546

    Google Scholar 

  • Capranica RR, Rose GJ, Brenowitz EA (1985) Time resolution in the auditory systems of anurans. In: Michelsen A (ed) Time resolution in auditory systems. Springer, Berlin Heidelberg New York Tokyo, pp 58–73

    Google Scholar 

  • Casseday JH, Covey E (1989) Inferior colliculus of the big brown bat: functional organization. In: Erber J, Menze R, Pflüger H-J, Todd D (eds) Neural mechanisms of behavior. Proceedingsof the 2nd International Congress of Neuroethology

  • Covey E, Hall WC, Kobler JB (1987) Subcortical connections of the superior colliculus in the mustache bat, Pteronotus parnellii. J Comp Neurol 263:179–197

    Google Scholar 

  • Dear SP, Suga N (1989) Representation of target range in the dorsolateral midbrain tegmentum of the big brown bat. Soc Neurosci Abstr 15:1293

    Google Scholar 

  • Dear SP, Haresign T, Ferragamo M, Fritz J, Moss CF, Simmons JA (1990) Response properties of neurons in the auditory cortex of the big brown bat. Soc Neurosci Abstr 16:718

    Google Scholar 

  • Epping WJM, Eggermont JJ (1986) Sensitivity of neurons in the auditory midbrain of the grasshopper to temporal characteristics of sound. II. Stimulation with amplitude modulated sounds. Hearing Res 24: 55–72

    Google Scholar 

  • Feng AS, Simmons JA, Kick SA (1978) Echo detection and targetranging neurons in the auditory system of the bat Eptesicus fuscus. Science 202:645–648

    Google Scholar 

  • Feng AS, Hall JC, Gooler DM (1990) Neural basis of sound pattern recognition in anurans. Prog Neurobiol 34:313–329

    Article  CAS  PubMed  Google Scholar 

  • Gerhardt HC, Doherty JA (1988) Acoustic communication in the gray treefrog, Hyla versicolor: evolutionary and neurobiological implications. J Comp Physiol A 162:261–278

    Google Scholar 

  • Goldman LJ, Henson OW Jr (1977) Prey recognition and selection by the CF-bat Pteronotus p. parnellii. Behav Ecol Sociobiol 2:411–419

    Google Scholar 

  • Griffin DR (1953) Bat sounds under natural conditions, with evidence for the echolocation of insect prey. J Exp Zool 123:435–466

    Google Scholar 

  • Griffin DR (1958) Listening in the dark. Yale Univ Press, New Haven, CT (Reprinted by Dover Publications, New York, 1974)

    Google Scholar 

  • Griffin DR (1962) Comparative studies of the orientation sounds of bats. Symp Zool Soc Lond 7:57–66

    Google Scholar 

  • Griffin DR, Webster FA, Michael CR (1960) The echolocation of flying insects by bats. Anim Behav 8:141–154

    Google Scholar 

  • Hall JC, Feng AS (1986) Neural analysis of temporally patterned sounds in the frog's thalamus: processing of pulse duration and pulse repetition rate. Neurosci Lett 63:215–220

    Google Scholar 

  • Henson OW Jr (1965) The activity and function of the middle ear muscles in echolocating bats. J Physiol (Lond) 180:871–887

    Google Scholar 

  • Jen PH-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 148:389–398

    Google Scholar 

  • Jen PH-S, Schlegel PA (1982) Auditory physiological properties of the neurons in the inferior colliculus of the big brown bat, Eptesicus fuscus. J Comp Physiol 147:351–363

    Google Scholar 

  • Jen PH-S, Suga N (1976) Coordinated activities of the middle-ear and laryngeal muscles in echolocating bats. Science 191:950–952

    Google Scholar 

  • Jen PH-S, Sun XD, Chen DM, Teng HB (1987) Auditory space representation in the inferior colliculus of the FM bat, Eptesicus fuscus. Brain Res 419:7–18

    Google Scholar 

  • Jen PH-S, Sun XD, Lin PJ-J (1989) Frequency and space representation in the primary auditory cortex of the FM bat, Eptesicus fuscus. J Comp Physiol A 165:1–14

    Google Scholar 

  • Kick SA (1982) Target detection by the echolocating bat, Eptesicus fuscus. J Comp Physiol 145:431–435

    Google Scholar 

  • Kick SA, Simmons JA (1984) Automatic gain control in the bat's sonar receiver and the neuroethology of echolocation. J Neurosci 4:2725–2737

    Google Scholar 

  • Langner G (1983) Evidence for neuronal periodicity detection in the auditory system of the guinea fowl: implications for pitch analysis in the time domain. Exp Brain Res 52:33–355

    Google Scholar 

  • Langner G, Schreiner CE (1988) Periodicity coding in the inferior colliculus of the cat. I. Neuronal mechanisms. J Neurophysiol 60:1799–1822

    Google Scholar 

  • Langner G, Schreiner CE, Merzenich MM (1987) Covariation of response latency and temporal resolution in the inferior colliculus of the cat. Hearing Res 31:197–202

    Google Scholar 

  • Maekawa M, Wong D (1990) FM neurons become delay-sensitive in the auditory cortex of the Myotis bat. Soc Neurosci Abstr 16:330.5

    Google Scholar 

  • Metzner W (1989) A possible neuronal basis for Doppler-shift compensation in echolocating horseshoe bats. Nature 341:529–532

    Google Scholar 

  • Michelsen A, Larsen ON, Surlykke A (1985) Auditory processing of temporal cues in insect songs: frequency domain or time domain? In: Michelsen A (ed) Time resolution in auditory systems. Springer, Berlin Heidelberg New York Tokyo, pp 3–27

    Google Scholar 

  • Nachtigall PE, Moore PWB (1988) Animal sonar: Processes and performance. Plenum Press, New York

    Google Scholar 

  • Novick A (1971) Echolocation in bats: Some aspects of pulse design. Am Sci 59:198–209

    Google Scholar 

  • Obrist M (1989) Individuelle Variabilität der Echoortung: Vergleichende Freilanduntersuchungen an vier vespertilioniden Fledermausarten Kanadas. Dissertation, Ludwig-Maximilians-Universität, München

    Google Scholar 

  • O'Neill WE, Suga N (1979) Target-range sensitive neurons in the auditory cortex of the mustached bat. Science 203:69–73

    Google Scholar 

  • Phillips DP (1989) Timing of spike discharges in cat auditory cortex neurons: Implications for encoding of stimulus periodicity. Hearing Res 40:137–146

    Google Scholar 

  • Phillips DP, Hall SE, Hollett JL (1989) Repetition rate and signal level effects on neuronal responses to brief tone pulses in cat auditory cortex. J Acoust Soc Am 86:2537–2549

    Google Scholar 

  • Plassmann W (1985) Coding of amplitude-modulated tones in the central auditory system of catfish. Hearing Res 17:209–217

    Google Scholar 

  • Poon PWF, Sun XD, Kamada T, Jen PH-S (1990) Frequency and space representation in the inferior colliculus of the FM bat, Eptesicus fuscus. Exp Brain Res 79:83–91

    Google Scholar 

  • Rees A, Møller AR (1983) Responses of neurons in the inferior colliculus of the rat to AM and FM tones. Hearing Res 10:301–330

    Google Scholar 

  • Reimer K (1987) Coding of sinusoidally amplitude modulated acoustic stimuli in the inferior colliculus of the rufous horseshoe bat, Rhinolophus rouxi. J Comp Physiol A 161:305–313

    Google Scholar 

  • Rose G (1986) A temporal-processing mechanism for all species? Brain Behav Evol 28:134–144

    Google Scholar 

  • Rose G, Capranica RR (1983) Temporal selectivity in the central auditory system of the leopard frog. Science 219:1087–1089

    Google Scholar 

  • Rose GJ, Capranica RR (1984) Processing amplitude-modulated sounds by the auditory midbrain of two species of toads: matched temporal filters. J Comp Physiol A 154:211–219

    Google Scholar 

  • Rose GJ, Capranica RR (1985) Sensitivity to amplitude modulated sounds in the anuran auditory system. J Neurophysiol 53:446–465

    Google Scholar 

  • Roverud RC (1989) A gating mechanism for sound pattern recognition is correlated with the temporal structure of echolocation sounds in the rufous horseshoe bat. J Comp Physiol A 166:243–249

    Google Scholar 

  • Roverud RC, Grinnell AD (1985a) Discrimination performance and echolocation signal integration requirements for target detection and distance discrimination in the CF/FM bat, Noctilio albiventris. J Comp Physiol A 156:447–456

    Google Scholar 

  • Roverud RC, Grinnell AD (1985b) 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

    Google Scholar 

  • Schildberger K (1984) Temporal selectivity of identified auditory neurons in the cricket brain. J Comp Physiol A 155:171–185

    Google Scholar 

  • Schnitzler HU, Henson OW Jr (1980) Performance of airborne animal sonar system. I. Microchiroptera. In: Busnel R-G, Fish JF (eds) Animal sonar systems. Plenum, New York, pp 109–181

    Google Scholar 

  • Schnitzler HU, Menne D, Kober R, Heblich K (1983) The acoustical image of fluttering insects in echolocating bats. In: Huber F, Markl H (eds) Neuroethology and behavioral physiology. Springer, Berlin Heidelberg New York, pp 235–250

    Google Scholar 

  • Schnitzler HU, Kalko E, Miller L, Surlykke A (1987) Hunting and echolocation behavior of Pipistrellus kuhli. J Comp Physiol A 161:267–274

    Google Scholar 

  • Schreiner CE, Langner G (1988) Periodicity coding in the inferior colliculus of the cat. II. Topographic organization. J Neurophysiol 60:1823–1840

    Google Scholar 

  • Schuller G (1979) Coding of small sinusoidal frequency and amplitude modulations in the inferior colliculus of ‘cf-fm’ bat, Rhinolophus ferrumequinum. Exp Brain Res 34:117–132

    Google Scholar 

  • Schuller G (1984) Natural ultrasonic echoes from wing beating insects are encoded by collicular neurons in the CF-FM bat, Rhinolophus ferrumequinum. J Comp Physiol A 155:121–128

    Google Scholar 

  • Schuller G, Radtke-Schuller S (1988) Neural control of vocalization in bats at peripheral to midbrain levels. In: Newman JD (ed) The physiological control of mammalian vocalization. Plenum, New York, pp 67–86

    Google Scholar 

  • Schuller G, Radtke-Schuller S (1990) Neural control of vocalization in bats: mapping of brainstem areas with electrical microstimulation eliciting species-specific echolocation calls in the rufous horseshoe bat. Exp Brain Res 79:192–206

    Google Scholar 

  • Simmons JA (1973) The resolution of target range by echolocating bats. J Acoust Soc Am 54:157–173

    Google Scholar 

  • Simmons JA (1989) A view of the world through the bat's ear: the formation of acoustic images in echolocation. Cognition 33:155–199

    Google Scholar 

  • Simmons JA, Grinnell AD (1988) The performance of echolocation: acoustic images perceived by echolocating bats. In: Nachtigall PE, Moore PWB (eds) Animal sonar processes and performance. Plenum, New York, pp 353–385

    Google Scholar 

  • Simmons JA, Stein RA (1980) Acoustic images in bat sonar: echolocation signals and the evolution of echolocation. J Comp Physiol 135:61–84

    Google Scholar 

  • Simmons JA, Fenton MB, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 203:16–21

    Google Scholar 

  • Simmons JA, Freedman EG, Stevenson SB, Chen L, Wohlgenant TJ (1989) Clutter inference and the integration time of echoes in the echolocating bat, Eptesicus fuscus. J Acoust Soc Am 86:1318–1332

    Google Scholar 

  • Simmons JA, Moss CF, Ferragamo M (1990) Convergence of temporal and spectral information into acoustic images of complex sonar targets perceived by the echolocating bat, Eptesicus fuscus. J Comp Physiol A 166:449–470

    Google Scholar 

  • Suga N, Jen PH-S (1975) Peripheral control of acoustic signals in the auditory system of echolocating bats. J Exp Biol 62:277–311

    Google Scholar 

  • Suga N, Jen PH-S (1977) Further studies on the peripheral auditory system of CF-FM bats specialized for fine frequency analysis of Doppler-shifted echoes. J Exp Biol 69:207–232

    Google Scholar 

  • Suga N, Schlegel PA (1972) Neural attenuation of responses to emitted sounds in echolocating bats. Science 177:82–84

    Google Scholar 

  • Suga N, Shimozawa T (1974) Site of neural attenuation of responses to self-vocalized sounds in echolocating bats. Science 183:1211–1213

    Google Scholar 

  • Sullivan WE (1982a) Neural representation of target distance in auditory cortex of the echolocating bat Myotis lucifugus. J Neurophysiol 48:1011–1032

    Google Scholar 

  • Sullivan WE (1982b) Possible neural mechanisms of target distance coding in auditory system of the echolocating bat Myotis lucifugus. J Neurophysiol 48:1033–1047

    Google Scholar 

  • Von der Emde G, Menne D (1989) Discrimination of insect wingbeat-frequencies by the bat Rhinolophus ferrumequinum. J Comp Physiol A 164:663–671

    Google Scholar 

  • Walkowiak W (1984) Neuronal correlates of the recognition of pulsed sound signals in the grass frog. J Comp Physiol A 155:57–66

    Google Scholar 

  • Webster FA, Brazier OG (1968) Experimental studies on echolocation mechanisms in bats. Aerospace Medical Res Lab WrightPatterson, Air Force Base, Ohio AD 73373

    Google Scholar 

  • Wu M, Jen PH-S (1991) Encoding of stimulus intensity by inferiocollicular neurons of the big brown bat, Eptesicus fuscus. Chinese J Physiol (in press)

  • Zhang SQ, Sun XD, Jen PH-S (1987) Anatomical study of neural projections to the superior colliculus of the FM bat, Eptesicus fuscus. Brain Res 416:375–380

    Google Scholar 

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Pinheiro, A.D., Wu, M. & Jen, P.H.S. Encoding repetition rate and duration in the inferior colliculus of the big brown bat, Eptesicus fuscus . J Comp Physiol A 169, 69–85 (1991). https://doi.org/10.1007/BF00198174

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