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Frequency and space representation in the primary auditory cortex of the frequency modulating batEptesicus fuscus

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Summary

  1. 1.

    Frequency and space representation in the auditory cortex of the big brown bat,Eptesicus fuscus, were studied by recording responses of 223 neurons to acoustic stimuli presented in the bat's frontal auditory space.

  2. 2.

    The majority of the auditory cortical neurons were recorded at a depth of less than 500 urn with a response latency between 8 and 20 ms (Fig. 1 B, C). They generally discharged phasically and had nonmonotonic intensity-rate functions (Fig. 3). The minimum threshold, (MT) of these neurons was between 8 and 82 dB sound pressure level (SPL). Half of the cortical neurons showed spontaneous activity. All 55 threshold curves are Vshaped and can be described as broad, intermediate, or narrow (Fig. 4A).

  3. 3.

    Auditory cortical neurons are tonotopically organized along the anteroposterior axis of the auditory cortex. High-frequency-sensitive neurons are located anteriorly and low-frequency-sensitive neurons posteriorly (Figs. 5, 6). An overwhelming majority of neurons were sensitive to a frequency range between 30 and 75 kHz (Fig. 1 A).

  4. 4.

    When a sound was delivered from the response center of a neuron on the bat's frontal auditory space, the neuron had its lowest MT. When the stimulus amplitude was increased above the MT, the neuron responded to sound delivered within a defined spatial area. The response center was not always at the geometric center of the spatial response area. The latter also expanded with stimulus amplitude (Fig. 8). High-frequency-sensitive neurons tended to have smaller spatial response areas than low-frequency-sensitive neurons (Figs. 7, 9).

  5. 5.

    Response centers of all 223 neurons were located between 0‡ and 50‡ in azimuth, 2‡ up and 25‡ down in elevation of the contralateral frontal auditory space (Fig. 10). Response centers of auditory cortical neurons tended to move toward the midline and slightly downward with increasing best frequency (BF; Fig. 11).

  6. 6.

    Auditory space representation appears to be systematically arranged according to the tonotopic axis of the auditory cortex. Thus, the lateral space is represented posteriorly and the middle space anteriorly (Fig. 12). Space representation, however, is less systematic in the vertical direction (Fig. 13).

  7. 7.

    Auditory cortical neurons are columnarly organized. Thus, the BFs, MTs, threshold curves, azimuthal location of response centers, and auditory spatial response areas of neurons sequentially isolated from an orthogonal electrode penetration are similar (Figs. 4, 7).

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Abbreviations

AC :

auditory cortex

BF :

best frequency

CF :

constant frequency

FM :

frequency modulated, modulating

MLD :

nucleus mesencephalicus lateralis dorsalis

MT :

minimum threshold

Q 10 BF:

divided by bandwidth of threshold curve at 10 dB above the MT

SPL :

sound pressure level

References

  • Asanuma A, Wong D, Suga N (1983) Frequency and amplitude representations in anterior primary auditory cortex of the mustache bat. J Neurophysiol 50:1182–1196

    Google Scholar 

  • Beranek LL (1954) Acoustics. Bolt, Beranek and Newman, Cambridge, MA (Reprinted by American Institute of Physics, 1986)

    Google Scholar 

  • Fuzessery ZM, Pollak GD (1984) Neural mechanisms of sound localization in an echolocating bat. Science 225:725–727

    Google Scholar 

  • Fuzessery ZM, Pollak GD (1985) Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study. J Neurophysiol 54:757–781

    Google Scholar 

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

    Google Scholar 

  • Grinnell AD (1963) The neurophysiology of audition in bats: directional localization and binaural interaction. J Physiol (Lond) 167:97–113

    Google Scholar 

  • Grinnell AD, Grinnell VS (1965) Neural correlates of vertical localization by echolocating bats. J Physiol (Lond) 181:830–851

    Google Scholar 

  • Henson OW (1970) The ear and audition. In: Wimsatt WA (ed) Biology of bats, vol. 2, Chap. 4. Academic, New York

    Google Scholar 

  • Hubel DH, Wiesel TN (1963) Shape and arrangement of columns in cat's striate cortex. J Physiol (Lond) 165:559–568

    Google Scholar 

  • Hubel DH, Wiesel TN (1974) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol 158:267–294

    Google Scholar 

  • Imig TJ, Adrian HO (1977) Binaural columns in the primary field (AI) of cat auditory cortex. Brain Res 138:241–257

    Google Scholar 

  • Imig TJ, Ruggero MA, Kitzes LM, Javel E, Brugge JF (1977) Organization of auditory cortex in the owl monkeyAotus trivirgatus. J Comp Neurol 171:111–128

    Google Scholar 

  • Jen PH-S (1974) Coding of directional information by single neurons in the superior olivary complex of echolocating bats. PhD thesis, Washington University, St. Louis

    Google Scholar 

  • Jen PH-S (1980) Coding of directional information by single neurons of the S-segment of the FM bat,Myotis lucifugus. J Exp Biol 87:203–216

    Google Scholar 

  • Jen PH-S, Chen DM (1988) Directionality of sound pressure transformation at the pinna of echolocating bats. Hearing Res 34:101–118

    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, Sun XD (1984) Pinna orientation determines the maximal directional sensitivity of bat auditory neurons. Brain Res 301:157–161

    Google Scholar 

  • Jen PH-S, Sun XD, Kamada T, Zhang SQ, Shimozawa T (1984a) Auditory response properties and spatial response areas of superior collicular neurons of the FM batEptesicus fuscus. J Comp Physiol A 154:407–413

    Google Scholar 

  • Jen PH-S, Kamada T, Sun XD, Schlegel P, Vater M, Harnischfeger G, Rübsamen R (1984b) Responses of cerebellar neurons to acoustic stimuli in certain FM and CF-FM bats. Chinese J Physiol 27:1–26

    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 

  • Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 9:1177–1194

    Google Scholar 

  • Knudsen EI, Konishi M (1978a) Space and frequency are represented separately in the auditory midbrain of the owl. J Neurophysiol 41:870–884

    Google Scholar 

  • Knudsen EI, Konishi M (1978b) A neural map of auditory space in the owl. Science 200:795–797

    Google Scholar 

  • Kujirai K, Suga N (1983) Tonotopic representation and space map in the non-primary auditory cortex of the mustached bat. Auris Nasus Larynx 10:9–24

    Google Scholar 

  • Lauter JL, Herscovitch P, Formby C, Raichle M (1985) Tonotopic organization in human auditory cortex revealed by positron emission tomography. Hearing Res 20:199–205

    Google Scholar 

  • Makous JC, O'Neill WE (1986) Directional sensitivity of the auditory midbrain in the mustached bat to free-field tones. Hearing Res 24:73–88

    Google Scholar 

  • Manabe T, Suga N, Ostwald J (1978) Aural representation in the Doppler-shifted-CF processing area of the primary auditory cortex of the mustached bat. Science 200:339–342

    Google Scholar 

  • Merzenich MM, Brugge JF (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res 50:275–296

    Google Scholar 

  • Merzenich MM, Knight PL, Roth GL (1975) Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231–249

    Google Scholar 

  • Michael CR (1981) Columnar organization of color cells in monkey's striate cortex. J Neurophysiol 46:587–604

    Google Scholar 

  • Mountcastle VB (1957) Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20:408–434

    Google Scholar 

  • Neuweiler G (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Gro\en HufeisennaseRhinolophus ferrumequinum. Z Vergl Physiol 67:273–306

    Google Scholar 

  • Ostwald J (1984) Tonotopical organization and pure tone response characteristics of single units in the auditory cortex of the greater horseshoe bat. J Comp Physiol A 155:821–834

    Google Scholar 

  • 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

    Google Scholar 

  • Pollak GD, Bodenhamer RD, Zook JM (1983) Cochleotopic organization of the mustache bat's inferior colliculus. In: Ewert JP, Capranica RR, Ingle DJ (eds) Advances in vertebrate neuroethology. New York. Plenum Press, pp 925–935

    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 

  • Reale RA, Imig TJ (1980) Tono topic organization in auditory cortex of the cat. J Comp Neurol 192:265–291

    Google Scholar 

  • Schlegel P (1977) Directional coding by binaural brainstem units of CF-FM bat,Rhinolophus ferrumequinum. J Comp Physiol 118:327–352

    Google Scholar 

  • Schlegel PA, Jen PH-S, Singh S (1988) Auditory spatial sensitivity of inferior collicular neurons in echolocating bats. Brain Res 456:127–138

    Google Scholar 

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

    Google Scholar 

  • Schweizer H (1981) The connections of the inferior colliculus and the organization of the brainstem auditory system in the greater horseshoe bat (Rhinolophus ferrumequinum). J Comp Neurol 201:25–49

    Google Scholar 

  • Shimozawa T, Suga N, Hendler P, Schuetze S (1974) Directional sensitivity of echolocation systems in bats producing frequency-modulated signals. J Exp Biol 60:53–59

    Google Scholar 

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

    Google Scholar 

  • Simmons JA, Fenton MD, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 2032:16–21

    Google Scholar 

  • Suga N (1964) Single unit activity in cochlear nucleus and inferior colliculus of echolocating bats. J Physiol 172:449–474

    Google Scholar 

  • Suga N (1965) Functional properties of auditory neurons in the cortex of echolocating bats. J Physiol 181:671–700

    Google Scholar 

  • Suga N (1977) Amplitude-spectrum representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustached bat. Science 196:64–67

    Google Scholar 

  • Suga N (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Edelman GM, Gall WE, Cowan WM (eds) Dynamic aspects of neocortical function. Wiley, New York, pp 315–373

    Google Scholar 

  • Suga N, Jen PH-S (1976) Disproportionate tonotopic representation for processing species-specific CF-FM sonor signals in the mustached bat auditory cortex. Science 194:542–544

    Google Scholar 

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

    Google Scholar 

  • Suga N, Manabe T (1982) Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J Neurophysiol 47:225–255

    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, Simmons JA, Jen PH-S (1975) Peripheral specialization for fine analysis of Doppler-shifted echoes in ‘CF-FM’ batPteronotus p. parnellii. J Exp Biol 63:161–192

    Google Scholar 

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

    Google Scholar 

  • Sun XD, Jen PH-S (1987) Pinna position affects the auditory space representation in the inferior colliculus of the FM bat,Eptesicus fuscus. Hear Res 27:207–219

    Google Scholar 

  • Sun XD, Jen PH-S, Kamada T (1983) Mapping of the auditory area in the cerebellar vermis and hemispheres of the mustache bat,Pteronotus parnellii parnellii. Brain Res 271:162–165

    Google Scholar 

  • Sun XD, Jen PH-S, Zhang WP (1987) Auditory spatial response areas of single neurons and space representation in the cerebellum of echolocating bats. Brain Res 414:314–322

    Google Scholar 

  • Taniguchi I, Arai O, Saito N (1988) Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats. Neurosci Lett 88:17–20

    Google Scholar 

  • Tunturi AR (1944) Audio frequency localization in the acoustic cortex of the dog. Am J Physiol 141:397–403

    Google Scholar 

  • Van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex. J Physiol 277:193–226

    Google Scholar 

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

    Google Scholar 

  • Wong D, Shannon SL (1988) Functional zones in the auditory cortex of the echolocating bat,Myotis lucifugus. Brain Res 453:349–352

    Google Scholar 

  • Woolsey CN, Walzl EM (1941) Topical projection of nerve fibers from local regions of the cochlea to the cerebral cortex of the cat. Am J Physiol 133:498–499

    Google Scholar 

  • Zook JM, Casseday JH (1982) Origin of ascending projections of inferior colliculus in the mustache bat,Pteronotus parnellii. J Comp Neurol 207:14–28

    Google Scholar 

  • 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 neural architecture. J Comp Neurol 231:530–546

    Google Scholar 

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Author notes

  1. Xinde Sun

    Present address: Department of Biology, East China Normal University, Shanghai, People's Republic of China

Authors and Affiliations

  1. Division of Biological Sciences, University of Missouri-Columbia, 65211, Columbia, Missouri, USA

    Philip H. -S. Jen, Xinde Sun & Paul J. J. Lin

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  1. Philip H. -S. Jen
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  2. Xinde Sun
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Jen, P.H.S., Sun, X. & Lin, P.J.J. Frequency and space representation in the primary auditory cortex of the frequency modulating batEptesicus fuscus . J. Comp. Physiol. 165, 1–14 (1989). https://doi.org/10.1007/BF00613794

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