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Auditory properties of the superior colliculus in the horseshoe bat, Rhinolophus rouxi

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Summary

Auditory response properties were studied in the superior colliculus (SC) of the echolocating horseshoe bat Rhinolophus rouxi, a long CF-FM bat, by the use of stationary, dichotic stimuli.

The most striking finding in the horseshoe bat was an enormous overrepresentation of neurons with best frequencies in the range of the constant frequency component of the species specific echolocation call (72% of the auditory neurons). These neurons had response thresholds as low as 0 dB SPL and were narrowly tuned with Q10 dB — values up to 400, just as in the nuclei of the primary auditory pathway in this species. This overrepresentation may suggest the importance of the superior colliculus in the context of echolocation behavior.

While noise stimuli were not particularly effective, other auditory response properties were similar to those described in other mammals. 65% of the SC neurons in the horseshoe bat responded only to monaural stimulation of one ear, primarily the contralateral one. 32% of the neurons received monaural input from both ears. The proportion of neurons responsive to ipsilateral stimulation (41%) was rather high. Mean response latency was 8.9 ms for contralateral stimulation.

A tonotopic organization is lacking, but high-frequency neurons are less frequent in rostral SC.

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Abbreviations

CF :

constant frequency component of echolocation call;

>CF :

frequencies above range of CF-component

FM :

frequency modulated component of echolocation call

<FM :

frequencies below range of FM-component

RF :

resting frequency of an individual bat

Rh.r. :

Rhinolophus rouxi

SC :

superior colliculus

References

  • Allom N, Wollberg Z (1978) Responses of cells in the superior colliculus of the squirrel monkey to auditory stimuli. Brain Res 159:321–330

    Google Scholar 

  • Carlile S, Pettigrew AG (1987) Distribution of frequency sensitivity in the superior colliculus of the guinea pig. Hearing Res 31:123–136

    Google Scholar 

  • Casagrande VA, Harting JK, Hall WC, Diamond IT, Martin GF (1972) Superior colliculus of the tree shrew: a structural and functional subdivision into superficial and deep layers. Science 177:444–447

    Google Scholar 

  • Casseday JH, Kobler JB, Isbey SF, Covey E (1989) Central acoustic tract in an echolocating bat: An extralemniscal auditory pathway to the thalamus. J Comp Neurol 287:247–259

    Google Scholar 

  • Chalupa LM, Rhoades RW (1977) Responses of visual, somatosensory, and auditory neurons in the golden hamster's superior colliculus. J Physiol 270:595–626

    Google Scholar 

  • Cotter JR (1985) Retinofugal projections of the big brown bat, Eptesicus fuscus, and the neotropical fruit bat, Artibeus jamaicensis. Am J Anat 172:105–124

    Google Scholar 

  • Cotter JR, Pentney RJP (1979) Retinofugal projections of nonecholocating (Pteropus giganteus) and echolocating (Myotis lucifugus) bats. J Comp Neurol 184:381–400

    Google Scholar 

  • 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 

  • Dean P, Redgrave P, Westby GWM (1989) Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:137–147

    Google Scholar 

  • Dräger UC, Hubel DH (1975) Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J Neurophysiol 38:690–713

    Google Scholar 

  • Edwards SB, Ginsburg CL, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184:309–330

    Google Scholar 

  • Feng AS, Vater M (1985) Functional organization of the cochlear nucleus of rufous horseshoe bats: frequencies and internal connections are arranged in slabs. J Comp Neurol 225:529–553

    Google Scholar 

  • Graham J, Pearson HE, Berman N, Murphy EH (1981) Laminar organization of superior colliculus in the rabbit: A study of receptive field properties of single units. J Neurophysiol 45:915–932

    Google Scholar 

  • Hirsch JA, Chan JCK, Yin TCT (1985) Responses of neurons in the cat's superior colliculus to acoustic stimuli: I. Monaural and binaural response properties, J Neurophysiol 53:726–745

    Google Scholar 

  • Huerta MF, Harting JK (1984) The mammalian superior colliculus: studies of its morphology and connections. In : Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New York, pp 687–773

    Google Scholar 

  • Jen PHS, Sun X, Kamada T, Zhang S, Shimozawa T (1984) Auditory response properties and spatial response areas of superior collicular neurons in the FM bat, Eptesicus fuscus. J Comp Physiol A 154:407–413

    Google Scholar 

  • King AJ, Hutchings ME (1987) Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: A map of auditory space. J Neurophysiol 57:596–624

    Google Scholar 

  • King AJ, Palmer AR (1983) Cells responsive to free field auditory stimuli in guinea pig superior colliculus: distribution and response properties. J Physiol 342:361–381

    Google Scholar 

  • Kobler JB, Isbey SF, Casseday JH (1987) Auditory pathways to the frontal cortex of the mustache bat, Pteronotus parnellii. Science 236:824–826

    Google Scholar 

  • Lund RD, Lund JS (1965) The visual system of the mole Talpa europaea. Exp Neurol 13:302–316

    Google Scholar 

  • Mast TE, Chung DY (1973) Binaural interactions in the superior colliculus of the chinchilla. Brain Res 62:227–230

    Google Scholar 

  • Metzner W (1988) Die funktioneile Bedeutung tegmentaler Neurone bei der Echoortung der Hufeisennase Rhinolophus rouxi. PhD thesis, Universität München

  • Metzner W, Radtke-Schuller S (1987) The nuclei of the lateral lemniscus in the rufous horseshoe bat, Rhinolophus rouxi. J Comp Physiol A 160:395–411

    Google Scholar 

  • Middlebrooks JC (1987) Binaural mechanisms of spatial tuning in the cat's superior colliculus distinguished using monaural occlusion. J Neurophysiol 57:688–701

    Google Scholar 

  • Middlebrooks JC, Knudsen EI (1984) A neural code for auditory space in the cat's superior colliculus. J Neurosci 4:2621–2634

    CAS  PubMed  Google Scholar 

  • Möller J, Neuweiler G, Zöller H (1978) Response characteristics of inferior colliculus neurons of the awake CF-FM bat Rhinolophus ferrumequinum I. Single tone stimulation. J Comp Physiol 125:217–225

    Google Scholar 

  • Neuweiler G (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Großen Hufeisennase Rhinolophus ferrumequinum. Z vergl Physiol 67:273–306

    Google Scholar 

  • Neuweiler G, Bruns V, Schuller G (1980) Ears adapted for the detection of motion, or how echolocating bats have exploited the capacities of the mammalian auditory system. J Acoust Soc Am 68:741–753

    Google Scholar 

  • Neuweiler G, Metzner W, Heilmann U, Rübsamen R, Eckrich M, Costa HH (1987) Foraging behavior and echolocation in the rufous horseshoe bat (Rhinolophus rouxi) of Sri Lanka. Behav Ecol Sociobiol 20:53–67

    Google Scholar 

  • Northmore DPM, Levine ES, Schneider GE (1988) Behavior evoked by electrical stimulation of the hamster superior colliculus. Exp Brain Res 73:595–605

    Google Scholar 

  • 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

    Google Scholar 

  • Palmer AR, King AJ (1985) A monaural space map in the guinea pig superior colliculus. Hearing Res 17:267–280

    Google Scholar 

  • Pentney RP, Cotter JR (1976) Retinofugal projections in an echolocating bat. Brain Res 115:479–484

    Google Scholar 

  • Pollak GD, Casseday JD (1989) The neural basis of echolocation in bats. Springer, Berlin Heidelberg, New York

    Google Scholar 

  • Poussin C, Schlegel P (1984) Directional sensitivity of auditory neurons in the superior colliculus of the bat, Eptesicus fuscus, using free field sound stimulation. J Comp Physiol A 154:253–261

    Google Scholar 

  • Rauschecker JP, Harris LR (1989) Auditory and visual neurons in the cat's superior colliculus selective for the direction of apparent motion stimuli. Brain Res 490:56–63

    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 

  • Reimer K (1989a) Retinofugal projections in the rufous horseshoe bat, Rhinolophus rouxi. Anat Embryol 180:89–98

    Google Scholar 

  • Reimer K (1989b) Bedeutung des Colliculus superior bei der Echoortung der Fledermaus Rhinolophus rouxi. PhD thesis, Universität München

  • Schlegel P (1977) Calibrated earphones for the echolocating bat, Rhinolophus ferrumequinum. J Comp Physiol 118:353–356

    Google Scholar 

  • Schuller G (1980) Hearing characteristics and Doppler-shift compensation in South Indian CF-FM bats. J Comp Physiol 139:349–356

    Google Scholar 

  • Schuller G, Pollak GD (1979) Disproportionate frequency representation in the inferior colliculus of Doppler compensating greater horseshoe bats: Evidence for an acoustic fovea. J Comp Physiol 132:47–54

    Google Scholar 

  • Schuller G, Beuter K, Schnitzler HU (1974) Response to frequency shifted artificial echoes in the bat, Rhinolophus ferrumequinum. J Comp Physiol 89:275–286

    Google Scholar 

  • Schuller G, Radtke-Schuller S, Betz M (1986) A stereotaxic method for small animals using experimentally determined reference profiles. J Neurosci Meth 18:339–350

    Google Scholar 

  • Schuller G, Covey E, Casseday JH (1991) Auditory pontine grey: connections and response properties in the horseshoe bat. Eur J Neurosci (submitted)

  • Simmons JA (1969) Acoustic radiation patterns for the echolocating bats Chilonycteris rubiginosa and Eptesicus fuscus J Acoust Soc Am 46:1054–1056

    Google Scholar 

  • Shimozawa T, Sun X, Jen PHS (1984) Auditory space representation in the superior colliculus of the big brown bat Eptesicus fuscus. Brain Res 311:289–296

    Google Scholar 

  • Sparks DL (1986) Translation of sensory signals into commands for control of saccadic eye movements: Role of primate superior colliculus. Physiol Rev 66:118–171

    Google Scholar 

  • Sparks DL (1988) Neural cartography: Sensory and motor maps in the superior colliculus. Brain Behav Evol 31:49–56

    Google Scholar 

  • Sparks DL, Nelson JS (1987) Sensory and motor maps in the mammalian superior colliculus. Trends Neurosci 10:312–317

    Google Scholar 

  • Stein BE (1984) Multimodal representation in the superior colliculus and optic tectum. In: Vanegas H (ed) Comparative neurology of the optic tectum. Plenum Press, New York, pp 819–841

    Google Scholar 

  • Sun X, Jen PHS, Kamada T (1983) Neurons in the superior colliculus of echolocating bats respond to ultrasonic signals. Brain Res 275:148–152

    Google Scholar 

  • Suthers R A, Braford MR (1980) Visual systems and the evolutionary relationships of the Chiroptera. Proc 5th Intern Bat Res Conf, pp 331–346

  • Tiao YC, Blakemore C (1976) Functional organization in the superior colliculus of the golden hamster. J Comp Neurol 168:483–504

    Google Scholar 

  • Wise LZ, Irvine DRF (1983) Auditory response properties of neurons in deep layers of cat superior colliculus. J Neurophysiol 3:674–685

    Google Scholar 

  • Wise LZ, Irvine DRF (1985) Topographic organization of interaural intensity difference sensitivity in deep layers of cat superior colliculus: implications for auditory spatial representation. J Neurophysiol 54:185–211

    Google Scholar 

  • Wong D (1984) Spatial tuning of auditory neurons in the superior colliculus of the echolocating bat, Myotis lucifugus. Hearing Res 16:261–270

    Google Scholar 

  • Wurtz RH, Albano JE (1980) Visual-motor functions of the primate superior colliculus. Annu Rev Neurosci 3:189–226

    Google Scholar 

Download references

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  1. Katrin Reimer

    Present address: Abteilung für Vergleichende Neurobiologie, Universität Ulm, Postfach 4066, W-7900, Ulm, Germany

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  1. Zoologisches Institut der Universität München, Luisenstraße 14, W-8000, München 2, Germany

    Katrin Reimer

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Reimer, K. Auditory properties of the superior colliculus in the horseshoe bat, Rhinolophus rouxi . J Comp Physiol A 169, 719–728 (1991). https://doi.org/10.1007/BF00194900

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