Journal of Comparative Physiology A

, Volume 165, Issue 1, pp 1–14 | Cite as

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

  • Philip H. -S. Jen
  • Xinde Sun
  • Paul J. J. Lin
Article

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).

     

Keywords

Sound Pressure Level Space Representation Auditory Cortex Response Center Primary Auditory Cortex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

AC

auditory cortex

BF

best frequency

CF

constant frequency

FM

frequency modulated, modulating

MLD

nucleus mesencephalicus lateralis dorsalis

MT

minimum threshold

Q10 BF

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

SPL

sound pressure level

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Asanuma A, Wong D, Suga N (1983) Frequency and amplitude representations in anterior primary auditory cortex of the mustache bat. J Neurophysiol 50:1182–1196Google Scholar
  2. Beranek LL (1954) Acoustics. Bolt, Beranek and Newman, Cambridge, MA (Reprinted by American Institute of Physics, 1986)Google Scholar
  3. Fuzessery ZM, Pollak GD (1984) Neural mechanisms of sound localization in an echolocating bat. Science 225:725–727Google Scholar
  4. Fuzessery ZM, Pollak GD (1985) Determinants of sound location selectivity in bat inferior colliculus: a combined dichotic and free-field stimulation study. J Neurophysiol 54:757–781Google Scholar
  5. Griffin DR (1958) Listening in the dark. Yale University Press, New Haven, CT (Reprinted by Dover Publications, New York, 1974)Google Scholar
  6. Grinnell AD (1963) The neurophysiology of audition in bats: directional localization and binaural interaction. J Physiol (Lond) 167:97–113Google Scholar
  7. Grinnell AD, Grinnell VS (1965) Neural correlates of vertical localization by echolocating bats. J Physiol (Lond) 181:830–851Google Scholar
  8. Henson OW (1970) The ear and audition. In: Wimsatt WA (ed) Biology of bats, vol. 2, Chap. 4. Academic, New YorkGoogle Scholar
  9. Hubel DH, Wiesel TN (1963) Shape and arrangement of columns in cat's striate cortex. J Physiol (Lond) 165:559–568Google Scholar
  10. Hubel DH, Wiesel TN (1974) Sequence regularity and geometry of orientation columns in the monkey striate cortex. J Comp Neurol 158:267–294Google Scholar
  11. Imig TJ, Adrian HO (1977) Binaural columns in the primary field (AI) of cat auditory cortex. Brain Res 138:241–257Google Scholar
  12. Imig TJ, Ruggero MA, Kitzes LM, Javel E, Brugge JF (1977) Organization of auditory cortex in the owl monkeyAotus trivirgatus. J Comp Neurol 171:111–128Google Scholar
  13. Jen PH-S (1974) Coding of directional information by single neurons in the superior olivary complex of echolocating bats. PhD thesis, Washington University, St. LouisGoogle Scholar
  14. Jen PH-S (1980) Coding of directional information by single neurons of the S-segment of the FM bat,Myotis lucifugus. J Exp Biol 87:203–216Google Scholar
  15. Jen PH-S, Chen DM (1988) Directionality of sound pressure transformation at the pinna of echolocating bats. Hearing Res 34:101–118Google Scholar
  16. 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 147:351–363Google Scholar
  17. Jen PH-S, Sun XD (1984) Pinna orientation determines the maximal directional sensitivity of bat auditory neurons. Brain Res 301:157–161Google Scholar
  18. 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 154:407–413Google Scholar
  19. 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 27:1–26Google Scholar
  20. 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 419:7–18Google Scholar
  21. Knudsen EI (1982) Auditory and visual maps of space in the optic tectum of the owl. J Neurosci 9:1177–1194Google Scholar
  22. Knudsen EI, Konishi M (1978a) Space and frequency are represented separately in the auditory midbrain of the owl. J Neurophysiol 41:870–884Google Scholar
  23. Knudsen EI, Konishi M (1978b) A neural map of auditory space in the owl. Science 200:795–797Google Scholar
  24. Kujirai K, Suga N (1983) Tonotopic representation and space map in the non-primary auditory cortex of the mustached bat. Auris Nasus Larynx 10:9–24Google Scholar
  25. Lauter JL, Herscovitch P, Formby C, Raichle M (1985) Tonotopic organization in human auditory cortex revealed by positron emission tomography. Hearing Res 20:199–205Google Scholar
  26. Makous JC, O'Neill WE (1986) Directional sensitivity of the auditory midbrain in the mustached bat to free-field tones. Hearing Res 24:73–88Google Scholar
  27. 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 200:339–342Google Scholar
  28. Merzenich MM, Brugge JF (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res 50:275–296Google Scholar
  29. Merzenich MM, Knight PL, Roth GL (1975) Representation of cochlea within primary auditory cortex in the cat. J Neurophysiol 38:231–249Google Scholar
  30. Michael CR (1981) Columnar organization of color cells in monkey's striate cortex. J Neurophysiol 46:587–604Google Scholar
  31. Mountcastle VB (1957) Modality and topographic properties of single neurons of cat's somatic sensory cortex. J Neurophysiol 20:408–434Google Scholar
  32. Neuweiler G (1970) Neurophysiologische Untersuchungen zum Echoortungssystem der Gro\en HufeisennaseRhinolophus ferrumequinum. Z Vergl Physiol 67:273–306Google Scholar
  33. 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 155:821–834Google Scholar
  34. Pollak GD, Bodenhamer RD (1981) Specialized characteristics of single units in inferior colliculus of mustache bat: frequency representation tuning, and discharge patterns. J Neurophysiol 46:605–620Google Scholar
  35. 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 925–935Google Scholar
  36. 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 154:253–261Google Scholar
  37. Reale RA, Imig TJ (1980) Tono topic organization in auditory cortex of the cat. J Comp Neurol 192:265–291Google Scholar
  38. Schlegel P (1977) Directional coding by binaural brainstem units of CF-FM bat,Rhinolophus ferrumequinum. J Comp Physiol 118:327–352Google Scholar
  39. Schlegel PA, Jen PH-S, Singh S (1988) Auditory spatial sensitivity of inferior collicular neurons in echolocating bats. Brain Res 456:127–138Google Scholar
  40. 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 132:47–54Google Scholar
  41. 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 201:25–49Google Scholar
  42. Shimozawa T, Suga N, Hendler P, Schuetze S (1974) Directional sensitivity of echolocation systems in bats producing frequency-modulated signals. J Exp Biol 60:53–59Google Scholar
  43. Shimozawa T, Sun XD, Jen PH-S (1984) Auditory space representation in the superior colliculus of the big brown bat,Eptesicus fuscus. Brain Res 311:289–296Google Scholar
  44. Simmons JA, Fenton MD, O'Farrell MJ (1979) Echolocation and pursuit of prey by bats. Science 2032:16–21Google Scholar
  45. Suga N (1964) Single unit activity in cochlear nucleus and inferior colliculus of echolocating bats. J Physiol 172:449–474Google Scholar
  46. Suga N (1965) Functional properties of auditory neurons in the cortex of echolocating bats. J Physiol 181:671–700Google Scholar
  47. Suga N (1977) Amplitude-spectrum representation in the Doppler-shifted-CF processing area of the auditory cortex of the mustached bat. Science 196:64–67Google Scholar
  48. 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 315–373Google Scholar
  49. Suga N, Jen PH-S (1976) Disproportionate tonotopic representation for processing species-specific CF-FM sonor signals in the mustached bat auditory cortex. Science 194:542–544Google Scholar
  50. 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 69:207–232Google Scholar
  51. Suga N, Manabe T (1982) Neural basis of amplitude-spectrum representation in auditory cortex of the mustached bat. J Neurophysiol 47:225–255Google Scholar
  52. Suga N, Schlegel PA (1972) Neural attenuation of responses to emitted sounds in echolocating bats. Science 177:82–84Google Scholar
  53. 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 63:161–192Google Scholar
  54. Sullivan WE (1982) Neural representation of target distance in auditory cortex of the echolocating batMyotis lucifugus. J Neurophysiol 48:1011–1032Google Scholar
  55. 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 27:207–219Google Scholar
  56. 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 271:162–165Google Scholar
  57. 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 414:314–322Google Scholar
  58. Taniguchi I, Arai O, Saito N (1988) Functional laminar and columnar organization of the auditory centers in echolocating Japanese greater horseshoe bats. Neurosci Lett 88:17–20Google Scholar
  59. Tunturi AR (1944) Audio frequency localization in the acoustic cortex of the dog. Am J Physiol 141:397–403Google Scholar
  60. Van Essen DC, Zeki SM (1978) The topographic organization of rhesus monkey prestriate cortex. J Physiol 277:193–226Google Scholar
  61. Wong D (1984) Spatial tuning of auditory neurons in the superior colliculus of the echolocating batMyotis lucifugus. Hearing Res 16:261–270Google Scholar
  62. Wong D, Shannon SL (1988) Functional zones in the auditory cortex of the echolocating bat,Myotis lucifugus. Brain Res 453:349–352Google Scholar
  63. 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 133:498–499Google Scholar
  64. Zook JM, Casseday JH (1982) Origin of ascending projections of inferior colliculus in the mustache bat,Pteronotus parnellii. J Comp Neurol 207:14–28Google Scholar
  65. 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 231:530–546Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • Philip H. -S. Jen
    • 1
  • Xinde Sun
    • 1
  • Paul J. J. Lin
    • 1
  1. 1.Division of Biological SciencesUniversity of Missouri-ColumbiaColumbiaUSA

Personalised recommendations