The Neocortex pp 137-157 | Cite as

Flying Cats and Flying Primates: Evolutionary Surprises from Neurobiology

  • John D. Pettigrew
Part of the NATO ASI Series book series (NSSA, volume 200)


In this chapter I use two papers (Pettigrew 1979; Pettigrew 1986) to show how one can illuminate evolutionary problems with the fine spotlight provided by modern neuroscientific investigations.


Receptive Field Superior Colliculus Striate Cortex Binocular Disparity Ocular Dominance 
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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  1. Frisby, J.P., and Mayhew, J.E.W. (1980) Spatial frequency tuned channels: implications for structure from psychophysical and computational studies of stereopsis. Phil. Trans. Roy. Soc. Lond. B., 290: 95–116.CrossRefGoogle Scholar
  2. Pettigrew, J.D. (1979) Binocular visual processing in the owl’s telencephalon. Proc. Roy. Soc. Lond. B, 204: 435–454.CrossRefGoogle Scholar
  3. Pettigrew, J.D. (1986) Flying primates? Megabats have the advanced pathway from eye to midbrain. Science, 231: 1304–1306.PubMedCrossRefGoogle Scholar
  4. Pettigew, J.D., Jamieson, B.G.M., Robson, S.K., Hall, L.S., McAnally, K.I., and Cooper, H.M. (1989) Phylogenetic relations between microbats, megabats and primates (Mammalia: Chi-roptera, Primates). Phil. Trans. Roy. Soc. Lond. B., 334: 1–70.Google Scholar
  5. Allman, J.M. (1977) Evolution of the visual system in the early primate. Prog. Psychobiol. Physiol Psychol. 7, 1–53.Google Scholar
  6. Allman, J.M., and Kaas, J. (1974) The organisation of the second visual area (V II) in the owl monkey: a second order transformation of the visual hemifield. Brain Res. 76, 247–265.PubMedCrossRefGoogle Scholar
  7. Barlow, H.B., Blakemore, C., and Pettigrew, J.D. (1967) The neural mechanism of binocular depth discrimination. J. Physiol, Lond. 193, 327–342.PubMedGoogle Scholar
  8. Blasdel, G.G., Mitchell, D.E., Muir, D.W., and Pettigrew, J.D. (1977) A physiological and behavioural study in cats of the effect of early visual experience with contours of a single orientation. J. Physiol., Lond. 265, 615–636.PubMedGoogle Scholar
  9. Bravo, H., and Pettigrew, J.D. (1979) A retrograde transport study of the neurones projecting to the primary visual nuclei of the owl, Speotyto cunicularia. In preparation.Google Scholar
  10. Clarke, P.G.H., Donaldson, I.M.L., and Whitteridge, D. (1976) Binocular visual mechanisms in cortical areas I and II of the sheep. J. Physiol., Lond. 256, 509–526.PubMedGoogle Scholar
  11. Cooper, M.L., and Pettigrew, J.D. (1979) A neurophysiological determination of the vertical horopter in cat and owl. J. Comp. Neurol., 184, 1–25.PubMedCrossRefGoogle Scholar
  12. Dreher, B. (1972) Hypercomplex cells in the cat’s striate cortex. Invest. Opthal. 11, 355–356.Google Scholar
  13. Friedmann, H. (1946) Ecological counterparts in birds. Scient. Mon. 43, 395–398.Google Scholar
  14. Hirschberger, W. (1967) Histologische Untersuchungen an den primären viseullen Zentren des Eulengehirnes und der retinalen Repräsentation in ihen. J. Orn., Lpz. 198, 187–202.CrossRefGoogle Scholar
  15. Hubel, D.H., and Wiesel, T.N. (1959) Receptive fields of single neurones in the cat’s striate cortex. J. Physiol., Lond. 148, 574–591.PubMedGoogle Scholar
  16. Hubel, D.H., and Wiesel, T.N. (1962) Receptive fields, binocular interaction and functional architecture in the cat’s visual cortex. J. Physiol., Lond. 160, 106–154.PubMedGoogle Scholar
  17. Hubel, D.H., and Wiesel, T.N. (1965) Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 28, 229–289.PubMedGoogle Scholar
  18. Hubel, D.H., and Wiesel, T.N. (1968) Receptive fields and functional architecture of monkey striate cortex. J. Physiol., Lond. 195, 215–243.PubMedGoogle Scholar
  19. Hubel, D.H., and Wiesel, T.N. (1970) Cells sensitive to binocular depth in area 18 of the macaque monkey cortex. Nature, Lond. 225, 41–42.CrossRefGoogle Scholar
  20. Karten, H.J., Hodos, W., Nauta, W.J., and Revzin, A.M. (1973) Neural connections of the ‘visual Wulst’ of the avian telencephalon. Experimental studies in the pigeon (Colwnba livia) and owl (Speotyto cunicularia). J. Comp. Neurol. 150, 253–278.PubMedCrossRefGoogle Scholar
  21. Linnaeus, C. (1758) Systerna Natura. Regnum Animals, 10th edn. Leipzig: Engelmann.Google Scholar
  22. Nelson, J.I. (1978) Does orientation domain inhibition play a role in visual cortex plasticity? Expl. Brain Res. 32, 293–298.CrossRefGoogle Scholar
  23. Nelson, J.I., Kato, H., and Bishop, P.O. (1977) Discrimination of orientation and position disparities by binocularly activated neurons in cat striate cortex. J. Neurophysiol. 40, 260–283.PubMedGoogle Scholar
  24. Palmer, L.A., and Rosenquist, A.C. (1974) Visual receptive fields of single striate cortical units projecting to the superior colliculus in the cat. Brain Res. 67, 27–42.PubMedCrossRefGoogle Scholar
  25. Pettigrew, J.D. (1973) Binocular neurones which signal change of disparity in area 18 of cat visual cortex. Nature, Lond. 241, 123–124.CrossRefGoogle Scholar
  26. Pettigrew, J.D. (1974) The effect of visual experience on the development of stimulus specificity by kitten cortical neurones. J. Physiol., Lond. 237, 49–74.PubMedGoogle Scholar
  27. Pettigrew, J.D. (1978) Stereoscopic visual processing. Nature, Lond. 273, 9–11.CrossRefGoogle Scholar
  28. Pettigrew, J.D. (1979) Structural organisation of the owl’s visual Wulst. In preparation.Google Scholar
  29. Pettigrew, J.D., and Konishi, M. (1976a) Neurons selective for orientation and binocular disparity in the visual Wulst of the barn owl (Tyto alba). Science, N.Y. 193, 675–678.CrossRefGoogle Scholar
  30. Pettigrew, J.D., and Konishi, M. (1976b) Effect of monocular deprivation on binocular neurones in the owl’s visual Wulst. Nature, Lond. 264, 753–754.CrossRefGoogle Scholar
  31. Pettigrew, J.D., Nikara, T.N., and Bishop, P.O. (1968) Binocular interaction on single units in cat striate cortex: simultaneous stimulation by single moving slit with receptive fields in correspondence. Expl. Brain Res. 6, 391–410.Google Scholar
  32. Poggio, G.F., and Fischer, B. (1977) Binocular interaction and depth sensitivity in striate and prestriate cortex of behaving rhesus monkey. J. Neurophysiol. 40, 1392–1405.PubMedGoogle Scholar
  33. Ramachandran, V.S., Clarke, P.G.H., and Whitteridge, D. (1977) Cells selective to binocular disparity in the cortex of newborn lambs. Nature, Lond. 268, 333–335.CrossRefGoogle Scholar
  34. Rodieck, R.W. (1979) Visual pathways in mammals. A. Rev. Neurobiol. 2. (In press).Google Scholar
  35. Rowe, M.H., and Stone, J. (1977) Naming of neurones: classification and naming of cat retinal ganglion cells. Brain, Behav. Evol. 14, 185–216.CrossRefGoogle Scholar
  36. Schiller, P.H., Finlay, B.L., and Volman, S.F. (1976) Quantitative studies of single-cell properties in monkey striate cortex. II. Orientation specificity and ocular dominance. J. Neurophysiol. 39, 1320–1333.PubMedGoogle Scholar
  37. Stone, J. (1965) The naso-temporal division of the cat’s retina. J. Comp. Neurol. 136, 585–600.Google Scholar
  38. Wathey, J., and Pettigrew, J.D. (1979) Visual optics in the barn owl, Tyto alba. In preparation.Google Scholar

References and Notes

  1. 1.
    J.M. Allman, Prog. Physiol. Psychol. 7, 1 (1977).Google Scholar
  2. 2.
    By this test and others, members of the Menotyphla, which includes the three shrew, Tupaia, are now excluded from the primates, although they are the primates’ closest “sister group” (1, 9).Google Scholar
  3. 3.
    Prosimian Galago [R.H. Lane, J.M. Allman, J.H. Kaas, F.M. Miezin, Brain Res. 60, 335 (1973)]PubMedCrossRefGoogle Scholar
  4. new world primates, Saimiri [S. Kadoya, L.R. Wolin, L.C. Massopust, J. Comp. Neurol. 142, 495 (1972)]; and Aotis [R.H. Lane et al, ibid.]CrossRefGoogle Scholar
  5. old world monkey, Macaca [M. Cynader and N. Berman, J. Neurophysiol. 35, 187 (1972)].PubMedGoogle Scholar
  6. 4.
    This is the “primitive” or plesiomorphous pattern [E.O. Wiley, Phlogenetics (Wiley, New York, 1981)].Google Scholar
  7. 5.
    Anurans [R.M. Gaze, Q. J. Exp. Physiol. 43, 209 (1958)]PubMedGoogle Scholar
  8. teleosts [H. Schwassman and L. Kruger, J. Comp. Neurol. 124, 113 (1965)]PubMedCrossRefGoogle Scholar
  9. birds [H. Bravo and J.D. Pettigrew, J. Comp. Neurol. 199, 419 (1981)]PubMedCrossRefGoogle Scholar
  10. lizard [B.S. Stein and N.S. Gaither, J. Comp. Neurol. 202, 69 (1981)].Google Scholar
  11. 6.
    Rodents: rat [K.S. Lashley, J. Comp. Neurol. 59, 341 (1934)]CrossRefGoogle Scholar
  12. squirrel [W.C. Hall, J.H. Kaas, H. Killackey, I.T. Diamond, J. Neurophysiol. 34, 437 (1971)]PubMedGoogle Scholar
  13. and ground squirrel [C.N. Woolsey, T.G. Carlton, J.H. Kaas, FJ. Earls, Vision Res. 11, 115 (1971)].PubMedCrossRefGoogle Scholar
  14. 7.
    Rabbit [A. Hughes, Docum. Ophthalmol. (DenHaag) 30, 33 (1971)].CrossRefGoogle Scholar
  15. 8.
    Cat [M. Straschill and K.P. Hoffman, Brain Res. 13, 274 (1972)].CrossRefGoogle Scholar
  16. 9.
    Opossum C. Rocha-Miranda, R. Mendez-Otero, A.S. Ramoa, E. Volchan, L.G. Gawryszewski, in Development of Visual Pathways in Mammals, J. Stone, B. Dreher, D. Rapaport, Eds. (Liss, New York, 1984), pp. 179–198].Google Scholar
  17. 10.
    Tree shrew [J.H. Kaas, J.K. Halting, R.W. Guillery, Brain Res. 65, 343 (1974)].PubMedCrossRefGoogle Scholar
  18. 11.
    W.K. Gregory, Bull. Am. Mus. Nat. Hist. 27, 332 (1910).Google Scholar
  19. 12.
    W.A. Wimsatt, Biology of Bats (Academic Press, New York, 1970).Google Scholar
  20. 13.
    M.B. Fenton, Rev. Biol. 59, 33 (1984).CrossRefGoogle Scholar
  21. 14.
    J.D. Smith, in Biology of Bats of the New World Family Phllostomatidae, R.J. Baker, J.K. Jones, Jr., D.C. Carter, Eds. (Texas Tech Press, Lubbock, 1976), part 1, pp. 49–69; in Major Patterns in Vertebrate Evolution, M.K. Hecht, P.C. Goody, B.M. Hecht, Eds. (Plenum, New York, 1977), pp. 427-438; in Proc. Fifth International Bat Research Conference, D.E. Wilson and A.L. Gardner, Eds. (Texas Tech Press, Lubbock, 1980), pp. 233-244.Google Scholar
  22. 15.
    In two animals supplementation with Nembutal (pentobarbitone sodium) was used.Google Scholar
  23. 16.
    In Pteropus and Macroderma the vertical meridian was horizontally displaced from the blind spot approximately 18° and 2°, respectively. These values can be obtained from Fig. 1, given that in Pteropus 1 mm-8.6° and in Macroderma 1 mm =16° on the retina.Google Scholar
  24. 17.
    T. Nikara, P.O. Bishop, J.D. Pettigrew, Exp. Brain Res. 6, 353 (1968).PubMedCrossRefGoogle Scholar
  25. 18.
    In Pteropus, sex to ten separate injections were made, totaling 1 to 1.5 μl of 20 percent of HRP or 1 percent WGA-HRP solution, to involve the complete retinal projection area of the superior colliculus. In the case of WGA-HRP, which is colorless at the concentration used, fast-green dye was added to help gauge the degree of diffusion. In Macroderma, whose superior colliculus is only 2 mm across, two injections of 0.3 μl each were sufficient to involve the whole structure.Google Scholar
  26. 19.
    M.L. Cooper and J.D. Pettigrew, J. Comp. Neurol. 184, 1 (1979).PubMedCrossRefGoogle Scholar
  27. 20.
    Most of the remaining unlabled retinal ganglion cells are retinothalamic ganglion cells projecting to the lateral geniculate nucleus (J.D. Pettigrew, M.L. Graydon, P. Giorgi, in preparation).Google Scholar
  28. 21.
    Most of the characters usually advanced to link megabats and microbats are associated with the flight adaptation [for example, characters 51 to 60 of M.J. Novacek, in Macromolecular Sequences in systematic and Evolutionary Biology, M. Goodman, Ed. (Plenum, New York, 1982)], pp. 3-41. Other characters are contestable, having evolved in other unrelated mammalian (for example, fetal membrane characters 61 to 63, ibid) or possibly representing plesiomorphous rather than synapomorphous characters (for example, 48 to 50, ibid.).Google Scholar
  29. 22.
    A third possibility is that the advanced mode of retinotectal organization arose first in meg achiropteran bats, some of which later lost their powers of flight and gave rise to the primates. The extensive and fairly continuous fossil record of primates makes this scenario highly unlikely [M. Archer, in Vertebrate Zoogeography and Evolution in Australasia, M. Archer and G. Clayton, Eds. (Hesperian Press, Perth, 1983), pp. 949–993Google Scholar
  30. F. Szalay and E. Delson, Evolution and History of the Primates (Academic Press, New York, 1979)].Google Scholar
  31. 23.
    J.D. Smith and A. Starrett, in Biology of Bats of the New World Family Phyllostomatidae, part 3, R.J. Baker, J.K. Jones, Jr., D.C. Carter, Eds. (Texas Tech Press, Lubbock, 1979), pp. 229–316; J.D. Pettigrew, K.S. Robson, K.I. McAnally, in preparation.Google Scholar
  32. 24.
    J.D. Smith and G. Madkour, in Proceedings of the Fifth International Bat Research Conference, D.E. Wilson and A.L. Gardner, Eds. (Texas Tech Press, Lubbock, 1980) pp. 347–365Google Scholar
  33. J.E. Hill and J.D. Smith, Bats: An Natural History (British Museum, London, 1984).Google Scholar
  34. 25.
    K. Padian, Paleobiology 9, 218 (1982); J.M.V.Google Scholar
  35. 26.
    M. Archer, in Archer and Clayton [in (22), pp. 633-807].Google Scholar
  36. 27.
    M. Novacek, Nature (London) 315, 140 (1985).CrossRefGoogle Scholar
  37. 28.
    S. Hand, in Archer and Clayton [in (22), pp. 851-904]; A. Walker, Nature (London) 223, 647 (1969).CrossRefGoogle Scholar
  38. 29.
    There may be corollary developments in the telencephalic visual processing of movements by primates accompanying the advances in retinotectal organization, such as the MT (middle-temporal) visual cortical area found in primates, but in no other mammals so far studied (1). By the diagnostic criteria for MT that it be located in the temporal lobe and recieve a major direct input from the primary visual cortex, this cortical area seems to be present in Pteropus [M.B. Calford et al., Nature (London) 313, 477 (1985)] but not in Mac-roderma (unpublished observations). The similarity of so many different and complex details of visual organization in primates and pteropids strengths the argument against parallel appearance of the two systems.CrossRefGoogle Scholar
  39. 30.
    J.E. Cronin and V.M. Sarich, in Recent Advances in Primatology, vol. 3, Evolution, DJ. Chivers and K.A. Joysey, Eds. (Academic Press, New York, 1978), pp. 287–288.Google Scholar
  40. 31.
    Supported by grants from the Australian Research Grants Scheme and the National Health and Medical Council of Australia. L. Wise and M. Calford helped with some of the electro-physiological recording experiments and provided critical comments on the manuscript. R. Collins provided expert technical assistance. Staff of the Conservation Commission of Northern Territory gave invaluable assistance in the collection of Macroderma, which were obtained under permit D85-5633.Google Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • John D. Pettigrew
    • 1
    • 2
  1. 1.Vision, Touch and Hearing Research CenterUniversity of QueenslandSt. LuciaAustralia
  2. 2.Beckman Laboratories Division of BiologyCalifornia Institute of TechnologyPasadenaUSA

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