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The Neocortex pp 119-136 | Cite as

Representational Geometries of Telencephalic Auditory Maps in Birds and Mammals

  • H. Scheich
Chapter
Part of the NATO ASI Series book series (NSSA, volume 200)

Abstract

The evolution of the mammalian as well as of the bird brain is highlighted by the parallel acquisition of a voluminous telencephalon. Yet the routes of morphological forebrain differentiation taken by the two forms are strikingly divergent. Birds lack a true cortex with its specific cell types and a segregation of gray and white matter areas is not conspicuous. Instead the telencephalic mass is entirely composed of basal forebrain nuclei and multiple and thick dorsal layers of stellate cells, the latter being separated by several thin fibrous laminae and crossed by diffuse fiber tracts. In the layers of this dorsal roof, traditionally misnamed “striatum”, local variations of cytoarchitecture are present but rarely with sharp boundaries. Only with modern connectivity studies it has been recognized over the past three decades that in spite of this low degree of overt organization the bird telencephalon follows a plan very similar to that of mammalian forms. This covers functional subsystems (including neocortical equivalents) and their intratelencephalic connections as well as connections with subtelencephalic structures (Karten, 1969). It is the aim of this contribution to characterize the functional organization of the auditory cortex analogue, Field L, of birds and to compare it to auditory cortex in the mongolian gerbil (Meriones unguiculatus). Field L of birds from various families has been studied in greater detail over the years in this laboratory and the gerbil has been chosen recently as a mammalian model which allows specific comparisons with bird auditory systems. These species share low frequency hearing with most space in the telencephalic auditory maps devoted to the analysis of frequencies below 10 kHz. In chicks and gerbil there seems to be no specialization for communication sounds greatly distorting the spatial organization of their auditory maps.

Keywords

Auditory Cortex Mongolian Gerbil Primary Auditory Cortex Medial Geniculate Body Guinea Fowl 
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.

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References

  1. Abeles, M., and Goldstein, M.H. Jr. (1970) Functional architecture in cat primary auditory cortex: Columnar organization and organization according to depth. J. Neurophysiol, 33: 172–187.PubMedGoogle Scholar
  2. Biederman-Thorson, M. (1970) Auditory responses of units in the ovoid nucleus and cerebrum (field L) of the ring dove. Brain Res., 24: 247–265.PubMedCrossRefGoogle Scholar
  3. Bohringer, R.C., and Rowe, M.J. (1977) The organization of the sensory and motor areas of the cerebral cortex in the platypus (Ornitorhynchus anatinus). J. Comp. Neurol., 174: 1–14.PubMedCrossRefGoogle Scholar
  4. Bonke, B.A., Bonke, D., and Scheich, H. (1979) Connectivity of the auditory forebrain nuclei in the guinea fowl (Numida meleagris). Cell Tissue Res., 200: 101–121.PubMedCrossRefGoogle Scholar
  5. Bonke, D., Scheich, H., and Langner, G. (1979) Responsiveness of units in the auditory neo-striatum of the guinea fowl (Numida meleagris) to species-specific calls and synthetic stimuli. I. Tonotopy and functional zones of field L. J. Comp. Physiol, 132: 242–255.CrossRefGoogle Scholar
  6. Braun, K., Scheich, H., Schachner, M., and Heizmann, C.W. (1985) Distribution of parvalbu-min, cytochrome oxidase activity and 14C-2-deoxyglucose uptake in the brain of the zebra finch. I. Auditory and vocal motor systems. Cell Tissue Res., 240: 101–115.CrossRefGoogle Scholar
  7. Ebbesson, S.O.E. (1980) The parcellation theory and its relation to interspecific variability in brain organization, evolutionary and ontogenetic development and neuronal plasticity. Cell Tissue Res., 213: 179–212.PubMedGoogle Scholar
  8. Ebner, F.F. (1969) A comparison of primitive forebrain organization in metatherian and euth-erian mammals. Ann. New York Acad. Sci., 167: 241–257.CrossRefGoogle Scholar
  9. Erulkar, S.C. (1955) Tactile and auditory areas in the brain of the pigeon. J. Comp. Neurol., 103: 421–457.PubMedCrossRefGoogle Scholar
  10. Faber, H., Braun, K., Zuschratter, W., and Scheich, H. (1989) System-specific distribution of zink in the chick brain. A light-and electron-microscopic study using the Timm method. Cell Tissue Res., 258: 241–251.CrossRefGoogle Scholar
  11. Gates, G.R., and Aitkin, L.H. (1982) Auditory cortex in the marsupial possum (Trichosurus vulpecula). Hear. Res., 7: 1–11.PubMedCrossRefGoogle Scholar
  12. Goldstein, M.H. Jr., and Knight, P.L. (1980) Comparative organization of mammalian auditory cortex. In: Comparative Studies Of Hearing In Vertebrates (Eds: A.N. Popper and R.R. Fay) Springer-Verlag, New York, pp. 375–398.CrossRefGoogle Scholar
  13. Haug, F.M.S. (1973) Heavy metals in the brain. A light microscopic study in the rat with Timm’s sulphide silver method. Methodological considerations and cytological and regional staining patterns. Adv. Anat. Embryol. Cell. Biol., 47: 1–71.Google Scholar
  14. Häusler, U.H.L. (1989) Die strukturelle und funktionelle Organisation der Hörbahn im caudalen Vorderhirn des Staren (Sturnus vulgaris, L.) Ph.D. Thesis, Technische Univerität München.Google Scholar
  15. Heil, P. (1989) Untersuchungen zur interauralen Organisation des auditorischen Systems und zur Physiologie und Topographie FM-sensitiver Neurone und ihren Beziehungen zur tono-topen Organisation des auditorischen Vorderhirns beim Haushuhn. Ph.D. Thesis, Technische Hochschule Darmstadt.Google Scholar
  16. Heil, P., Langner, G., and Scheich, H. (1987) Neuronal responses in field L at the upper hearing limit of the chick. In: New Frontiers in Brain Research, Proc. 15th Göttinger Neurobiology Conference, Eds: N. Eisner and O. Creutzfeldt, Thieme-Verlag, Stuttgart, New York, p. 128.Google Scholar
  17. Heil, P., and Scheich, H. (1985) Quantitative analysis and two-dimensional reconstruction of the tonotopic organization of the auditory field L in the chick from 2-deoxyglucose data. Exp. Brain Res., 58: 532–543.PubMedCrossRefGoogle Scholar
  18. Heil, P., and Scheich, H. (1986) Effects of unilateral and bilateral cochlea removal on 2-deox-yglucose patterns in the chick auditory system. J. Comp. Neurol., 252: 279–301.PubMedCrossRefGoogle Scholar
  19. Hose, B. (1987) Neuronale Verarbeitung und topographische Repräsentation sprachrelevanter zeitlicher Parameter im auditorischen Vorderhirn von Beos (Gracula religiosa). Ph.D. Thesis, Technische Hochschule Darmstadt.Google Scholar
  20. Hose, B., Langner, G., and Scheich, H. (1987) Topographic representation of periodicities in the forebrain of the mynah bird: One map for pitch and rhythm? Brain Res., 422: 367–373.PubMedCrossRefGoogle Scholar
  21. Hubel, D.H., Wiesel, T.N., and Stryker, M.P. (1977) Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique. Nature, 269: 328–330.PubMedCrossRefGoogle Scholar
  22. Imig, T.J., Ruggero, M.A., Kitzes, L.M., Javel, E., and Brugge, J.F. (1977) Organization of auditory cortex in the owl monkey (Artus trivirgatus). J. Comp. Neurol., 171: 111–128.PubMedCrossRefGoogle Scholar
  23. Imig, T.J., and Reale, R.A. (1980) Patterns of cortico-cortical connections related to tonotopic maps in cat auditory cortex. J. Comp. Neurol., 192: 293–332.PubMedCrossRefGoogle Scholar
  24. Karten, H.J. (1968) The ascending auditory pathway in the pigeon (Colwnba livid). H. Telencephalic projections of the nucleus ovoidalis thalami. Brain Res., 11: 134–153.PubMedCrossRefGoogle Scholar
  25. Karten, H. J. (1969) The organization of the avian telencephalon and some speculations on the phylogeny of the amniote telencephalon. Ann. N.Y. Acad. Sci., 167: 164–179.CrossRefGoogle Scholar
  26. 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: 333–355.PubMedCrossRefGoogle Scholar
  27. Langner, G., Bonke, D., and Scheich, H. (1981) Neuronal discrimination of natural and synthetic vowels in field L of trained mynah birds. Exp. Brain Res., 43: 11–24.PubMedCrossRefGoogle Scholar
  28. Lende, R. A. (1969) A comparative approach to the neocortex: Localization in monotremes, marsupials and insectivores. Ann. New York Acad. Sci., 167: 262–276.CrossRefGoogle Scholar
  29. Leppelsack, H.-J. (1974) Funktionelle Eigenschaften der Hörbahn in Feld L des Neostriatum caudale des Staren. J. Comp. Physiol., 88: 271–320.CrossRefGoogle Scholar
  30. Luethke, L.E., Krubitzer, L.A., and Kaas, J.H. (1988) Cortical connections of electrophysiologi-cally and architectonically defined subdivisions of auditory cortex in squirrel. J. Comp. Neurol., 268: 181–203.PubMedCrossRefGoogle Scholar
  31. Macko, K.A., Jarvis, CD., Kennedy, C., Miyaoka, M., Shinohara, M., Sokoloff, L., and Miskin, M. (1982) Mapping the primate visual system with [2-14C] Deoxyglucose. Science, 218: 394–397.PubMedCrossRefGoogle Scholar
  32. Mata, M., Fink, DJ., Gainer, H., Smith, C.B., Davidsen, L., Savaki, H., Schwartz, W.J., and Sokoloff, L. (1980) Activity-dependent energy metabolism in rat posterior pituitary primarily reflects sodium pump activity. J. Neurochem., 34: 213–215.PubMedCrossRefGoogle Scholar
  33. McCashland, J.S., and Woolsey, T.A. (1988) High-resolution-2-deoxyglucose mapping of functional cortical columns in mouse barrel cortex. J. Comp. Neurol., 278: 555–569.CrossRefGoogle Scholar
  34. Merzenich, M.M., Anderson, R.A., and Middlebrooks, J.C. (1979) Functional and topographic organization of the auditory cortex. Exp. Brain Res., Suppl. (2): 61–75.CrossRefGoogle Scholar
  35. Merzenich, M.M., and Brugge, J.F. (1973) Representation of the cochlear partition on the superior temporal plane of the macaque monkey. Brain Res., 50: 275–296.PubMedCrossRefGoogle Scholar
  36. Middlebrooks, J.C., Dykes, R.W., and Merzenich, M.M. (1980) Binaural response-specific bands in primary auditory cortex (AI) of the cat: topographic organization orthogonal to isofrequency contours. Brain Res., 181: 31–48.PubMedCrossRefGoogle Scholar
  37. Müller, S.C., and Scheich, H. (1985) Functional organization of the avian auditory field L. A comparative 2DG study. J. Comp. Physiol., A156: 1–12.CrossRefGoogle Scholar
  38. Nudo, R.J., and Masterton, B. (1986) Stimulation-induced 14C-2-deoxyglucose labelling of synaptic activity in the central auditory system. J. Comp. Neurol., 245: 553–565.PubMedCrossRefGoogle Scholar
  39. Rose, M. (1914) Über die cytoarchitektonische Gliederung des Vorderhirns der Vögel. J. Psychol. Neurol. (Lpz) 21: 278–352.Google Scholar
  40. Ryan, A.F., Woolf, N.K., and Sharp, F.R. (1982) Tonotopic organization in the central auditory pathway of the mongolian gerbil: A 2-deoxyglucose study. J. Comp. Neurol., 207: 369–380.PubMedCrossRefGoogle Scholar
  41. Sachs, M.S., Woolf, N.K., and Sinott, J.M. (1980) Response properties of neurons in theavian auditory system: Comparisons with mammalian homologues and consideration of the encoding of complex stimuli. In: Comparative Studies of Hearing In Vertebrates. Eds: A.N. Popper and R.R. Fay, Springer-Verlag, New York: pp. 323–353.CrossRefGoogle Scholar
  42. Saini, K.D., and Leppelsack, H J. (1981) Cell types of the auditory caudomedial neostriatum of the starling, Sturnus vulgaris. J. Comp. Neurol., 198: 209–229.PubMedCrossRefGoogle Scholar
  43. Scheich, H. (1977) Central processing of complex sounds and feature analysis. In: Recognition of Complex Acoustic Signals. Ed: T.H. Bullock, Dahlem Konferenzen, Berlin: pp. 161-182.Google Scholar
  44. Scheich, H. (1983) Two columnar systems in the auditory neostriatum of the chick: Evidence from 2-deoxyglucose. Exp. Brain Res., 51: 199–205.PubMedCrossRefGoogle Scholar
  45. Scheich, H. (1985) Auditory brain organization of birds and its constraints for the design of vocal repertoires. In: Fortschritte der Zoologie, Eds: Lindauer and Hölldobler, Bd. 31, Experimental Behavioral Ecology, G. Fischer-Verlag, Stuttgart, New York: pp. 195–209.Google Scholar
  46. Scheich, H., Bonke, B.A., Bonke, D., and Langner, G. (1979b) Functional organization of some auditory nuclei in the guinea fowl demonstrated by the 2-deoxyglucose technique. Cell Tissue Res., 204: 17–27.PubMedCrossRefGoogle Scholar
  47. Scheich, H., Langner, G., and Bonke D (1979a) Responsiveness of units in the auditory neostriatum of the guinea fowl (nwnida meleagris) to species-specific calls and synthetic stimuli. II. Discriminatiuon of iambus-like calls. J. Comp. PhysioL, 132: 257–276.CrossRefGoogle Scholar
  48. Scheich, H., Langner, G., Tidemann, C., Coles, R.B., and Guppy, A. (1986) Electroreception and electrolocalization in platypus. Nature, 319: 401–402.PubMedCrossRefGoogle Scholar
  49. Schreiner, C.F., and Cynader, M.S. (1984) Basic functional organization of second auditory cortical field (AII) of the cat. J. Neurophysiol., 51: 1284–1305.PubMedGoogle Scholar
  50. Schreiner, CF., and Urbas, J.V. (1986) Representation of amplitude modulation in the auditory cortex of the cat I. The anterior auditory field (AAF). Hearing Res., 21: 227–241.CrossRefGoogle Scholar
  51. Steffen, H., Simonis, C., Thomas, H., Tillein, J., and Scheich, H. (1988) Auditory cortex: Multiple fields, their architectonics and connections in the mongolian gerbil. In: Auditory Pathway, Structures and Functions. Eds.: J. Syka and B. Masterton. Plenum Press, New York: pp. 223–228.CrossRefGoogle Scholar
  52. Suga, N. (1982) Functional organization of the auditory cortex: Representation beyond tono-topy in the bat. In: Cortical Sensory Organization. Vol. 3. Multiple Auditory Areas (Ed: C.N. Woolsey). Humana Press, Clifton, New Jersey, pp. 157–218.Google Scholar
  53. Theurich, M., Langner, G., and Scheich, H. (1984b) Infrasound responses in the midbrain of the guinea fowl. Neurosci. Lett., 49: 81–86.PubMedCrossRefGoogle Scholar
  54. Theurich, M., Müller, CM., and Scheich, H. (1984a) 2-deoxyglucose accumulation parallels extracellularly recorded spike activity in the avian auditory neostriatum. Brain Res., 322: 157–161.PubMedCrossRefGoogle Scholar
  55. Thomas, H. (1989) Funktionelle und anatomische Organisation des auditorischen Cortex beim Gerbil (Meriones unguiculatus). Ph.D. Thesis, Technische Hochschule Darmstadt.Google Scholar
  56. Tootell, R.B.H., Hamilton, S.L., Silverman, M.S., and Switkes, E. (1988) Functional anatomy of macaque striate cortex. I, II, IE, IV, V. J. Neurosci., 8: 1500–1624.PubMedGoogle Scholar
  57. Webster W.R., Serviáre, J., Batini, C., and Laplante, S. (1978) Autoradiographic demonstration with 2-[14C]deoxyglucose of frequency selectivity in the auditory system of cats under conditions of functional activity. Neurosci. Letters, 10: 43–48.CrossRefGoogle Scholar
  58. Wong-Riley, M., and Riley, D.A. (1983) The effect of impulse blockage on cytochrome oxidase activity in the cat visual system. Brain Res., 261: 185–193.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • H. Scheich
    • 1
  1. 1.Zoological InstituteTechnical University DarmstadtDarmstadtGermany

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