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Reconstructing the Evolution of the Brain in Primates Through the Use of Comparative Neurophysiological and Neuroanatomical Data

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Primate Brain Evolution

Abstract

In his influential book, The Antecedents of Man, Le Gros Clark (1962) maintained that the order Primates cannot be defined by specific attributes that uniquely distinguish its members from the members of other orders but rather can only be characterized by evolutionary trends such as the progressive expansion of the brain. Recent neurophysiological and neuroanatomical data suggest that at least one unique defining feature for the order Primates does exist. In all mammals the retina projects to the optic tectum, but the manner in which the visual field is represented in the optic tectum of Primates differs from that found in all other mammals. In Primates the optic tectum on each side of the brain contains a systematic representation of the contralateral half of the visual field, whereas in other mammals the optic tectum of each side contains a systematic representation of the visual field that is viewed by the contralateral retina, which is the primitive vertebrate condition found in all non-mammalian vertebrates (see Fig. 1). The drawback in using such neurophysiological criteria in taxonomic definitions is that it is not possible to survey a very large number of species for a particular attribute, and the method cannot be applied to fossils.

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References

  • Aggleton, J.P., Burton, M.J., and Passingham, R.E., 1980, Cortical and subcortical afferents to the amygdala of the rhesus monkey (Macaca mulatta). Brain Res., 190:347–368.

    Article  Google Scholar 

  • Allman, J.M., 1977. Evolution of the visual system in the early primates. In, Progress in Psychobiology, Physiology and Psychology, vol. 7, J.M. Sprague and A.N. Epstein, eds., Academic Press, New York.

    Google Scholar 

  • Allman, J.M., and Kaas, J.H., 1971a, A representation of the visual field in the caudal third of the middle temporal gyrus of the owl monkey (Aotus trivirgatus). Brain Res., 31:84–105.

    Article  Google Scholar 

  • Allman, J.M., and Kaas, J.H., 1971b, Representation of the visual field in striate and adjoining cortex of the owl monkey (Aotus trivirgatus). Brain Res., 35:89–106.

    Article  Google Scholar 

  • Allman, J.M., and Kaas, J.H., 1974a, The organization of the second visual area (V-II) in the owl monkey: A second order transformation of the visual hemifield. Brain Res., 76:247-265. Allman, J.M., and Kaas, J.H., 1974b. A crescent-shaped cortical visual area surrounding the middle temporal area (MT) in the owl monkey (Aotus trivirgatus). Brain Res., 81:199–213.

    Article  Google Scholar 

  • Allman, J.M., and Kaas, J.H., 1975, The dorsomedial cortical visual area: A third tier area in the occipital lobe of the owl monkey (Aotus trivirgatus). Brain Res., 100:473–487.

    Article  Google Scholar 

  • Allman, J.M., and Kaas, J.H., 1976, Representation of the visual field on the medial wall of occipital-parietal cortex in the owl monkey, Science, 191:572–575.

    Article  Google Scholar 

  • Allman, J.M., Campbell, C.B.G., and McGuinness, E., 1979, The dorsal third tier area in Galago senegalensis. Brain Res., 179:355–361.

    Article  Google Scholar 

  • Allman, J.M., Kaas, J.H., and Lane, R.H., 1973, The middle temporal visual area (MT) in the bushbaby, Galago senegalensis. Brain Res., 57:197–202.

    Article  Google Scholar 

  • Baker, J.F., Gibson, A., Glickstein, M., and Stein, J., 1976, Visual cells in the pontine nuclei of the cat. J. Physiol. (Lond.), 255:415–433.

    Google Scholar 

  • Baker, J.F., Petersen, S.E., Newsome, W.T., and Allman, J.M., 1981, Visual response properties of neurons in four extrastriate visual areas of the owl monkey (Aotus trivirgatus). A quantitative comparison of the medial (M), dorsomedial (DM), dorsolateral (DL), and middle temporal (MT) areas. J. Neurophysiol., 45:397–416.

    Google Scholar 

  • Bodian, D., 1937, An experimental study of the optic tracts and retinal projection of the Virginia opossum. J. Comp. Neurol., 66:133–144.

    Article  Google Scholar 

  • Campbell, C.B.G., 1966, The relationships of tree shrews: The evidence of the nervous system. Evolution, 20:276–281.

    Article  Google Scholar 

  • Campbell, C.B.G., 1974, On the phyletic relationships of tree shrews. Mammal Rev., 4:125–143.

    Article  Google Scholar 

  • Campbell, C.B.G., and Hayhow, W.R., 1971, Primary optic pathways in the echidna, Tachyglossus aculeatus: An experimental degeneration study. J. Comp. Neurol., 143:119–136.

    Article  Google Scholar 

  • Campbell, C.B.G., Jane, J.A., and Yashon, D., 1967, The retinal projections of the tree shrew and hedgehog. Brain Res., 5:406–418.

    Article  Google Scholar 

  • Campos-Ortega, J.A., 1970, The distribution of retinal fibres in the brain of the pig. Brain Res., 19:306–312.

    Article  Google Scholar 

  • Campos-Ortega, J.A., and Glees, P., 1967, The termination of ipsilateral and contralateral optic fibers in the lateral geniculate body of Galago crassicaudatus. J. Comp. Neurol., 129:279–284.

    Article  Google Scholar 

  • Cartmill, M., 1972. Arboreal adaptations and the origin of the order Primates, In, The Functional and Evolutionary Biology of Primates, R. H. Tuttle, ed., Aldine, Atherton, Chicago, pp. 97–122.

    Google Scholar 

  • Cartmill, M., 1974, Rethinking primate origins. Science, 184:436–443.

    Article  Google Scholar 

  • Cartmill, M., 1975. Primate Origins, Burgess, Minneapolis.

    Google Scholar 

  • Clutton-Brock, T.H., and Harvey, P.H., 1980, Primates, brains and ecology. J. Zool. (Lond.), 190:309–323.

    Article  Google Scholar 

  • Cummings, J.F., and de Lahunta, A., 1969, An experimental study of the retinal projections in the horse and sheep. Ann. N.Y. Acad. Sci., 157:293–318.

    Article  Google Scholar 

  • Cynader, M., and Berman, N., 1972, Receptive field organization of monkey superior colliculus. J. Neurophysiol., 35:187–201.

    Google Scholar 

  • DeBruyn, E.J., Wise, V.L., and Casagrande, V.A., 1980, The size and topographic arrangement of retinal ganglion cells in the Galago. Vision Res., 20:315–328.

    Article  Google Scholar 

  • Desimone, R., and Gross, C.G., 1979, Visual area: the temporal artery of the macque, Brain Res., 178:363–380.

    Article  Google Scholar 

  • Desimone, R., and Gross, C.G., 1980, Visual properties of inferior temporal cortex in the macaque. Exp. Brain Res., 41:818–819.

    Google Scholar 

  • Desimone, R., Fleming, J., and Gross, C.G., 1980, Prestriate afferents to inferior temporal cortex: an HRP study. Brain Res., 184:41–55.

    Article  Google Scholar 

  • Drager, U., 1974, Autoradiography of tritiated proline and fucose transported transneuronally from the eye to the visual cortex in pigmented and albino mice. Brain Res., 82:284–292.

    Article  Google Scholar 

  • Drager, U., and Hubel, D.H., 1975, Responses to visual stimulation and relationship between visual, auditory and somatosensory inputs in mouse superior colliculus. J. Neurophysiol., 38:690–713.

    Google Scholar 

  • Feldon, S., Feldon, P., and Kruger, L., 1970, Topography of the retinal projection upon the superior colliculus of the cat. Vision Res., 10:135–143.

    Article  Google Scholar 

  • Gaze, R.M., 1958, The representation of the retina on the optic lobe of the frog. Quart. J. Exp. Physiol., 43:209–214.

    Google Scholar 

  • Giolli, R.A., and Guthrie, M.D., 1969, The primary optic projections in the rabbit. An experimental degeneration study. J. Comp. Neurol., 136:99–126.

    Article  Google Scholar 

  • Giolli, R.A., and Tigges, J., 1970. The primary optic pathways and nuclei of primates. In, The Primate Brain, C.R. Noback and W. Montagna, eds., Appleton-Century-Crofts, New York, pp. 29–54.

    Google Scholar 

  • Glickstein, M., Cohen, J., Dixon, B., Gibson, A., Hollins, M., La Bossiere, E., and Robinson, F., 1980, Corticopontine visual projection in the macaque monkey. J. Comp. Neurol., 190:209–230.

    Article  Google Scholar 

  • Gross, C.G., 1973, Inferotemporal cortex and vision. Prog. Physiol. Psychol., 5:77–115.

    Google Scholar 

  • Gross, C.G., Bruce, C.J., Desimone, R., Fleming, J., and Gattas, R., 1981. Three visual areas of the temporal lobe. In, Multiple Cortical Areas, C.N. Woolsey, ed., Humana Press, Englewood Cliffs, N.J., in press.

    Google Scholar 

  • Heric, T.M., and Kruger, L., 1965, Organization of the visual projection upon the optic tectum of a reptile (Alligator mississippiensis). J. Comp. Neurol., 124:101–111.

    Article  Google Scholar 

  • Hershkovitz, P., 1977. Living New World Monkeys (Platyrrhini), vol. 1, Univ. Chicago Press, Chicago.

    Google Scholar 

  • Hill, W.C.O., 1953. Primates. Comparative Anatomy and Taxonomy. I. Strepsirhini, University of Edinburgh Press, Edinburgh.

    Google Scholar 

  • Hubel, D.H., LeVay, S., and Wiesel, T.N., 1975, Mode of termination of retinotectal fibers in macaque monkey: An autoradiographic study. Brain Res., 96:25–40.

    Article  Google Scholar 

  • Imig, T.J., Ruggero, M.A., Kitzes, L.M., Javel, E., and Brugge, J.F., 1977, Organization of auditory cortex in the owl monkey (Aotus trivirgatus). J. Comp. Neurol., 171:111–128.

    Article  Google Scholar 

  • Innis, R.B., Correa, F.M.A., Uhl, G.R., Schneider, B., and Snyder, S.H., 1979, Cholecystokinin octapeptide-like immunoreactivity: Histochemical localization in rat brain. Proc. Natl. Acad. Sci. USA, 76:521–525.

    Article  Google Scholar 

  • Jacobson, M., 1962, The representation of the retina on the optic tectum of the frog. Correlation between retinotectal magnification factor and retinal ganglion cell count. Quart. J. Exp. Physiol., 47:170–178.

    Google Scholar 

  • Jacobson, M., and Gaze, R.M., 1965, Types of visual response from single units in the optic tectum and optic nerve of goldfish. Quart. J. Exp. Physiol., 49:199–209.

    Google Scholar 

  • Jerison, H.J., 1973. Evolution of the Brain and Intelligence, Academic Press, New York.

    Google Scholar 

  • Kaas, J.H., Guillery, R.W., and Allman, J.M., 1972. Some principles of organization in the dorsal lateral geniculate nucleus. Brain Behav. Evol., 6;253–299.

    Article  Google Scholar 

  • Kaas, J.H., Hall, W.C., and Diamond, I.T., 1970, Cortical visual areas I and II in the hedgehog: Relation between evoked potential maps and architectonic subdivisions. J. Neurophysiol., 33:595–615.

    Google Scholar 

  • Kadoya, S., Wolin, L.R., and Massopust, L.C., 1971, Photically evoked unit activity in the tectum opticum of the squirrel monkey. J. Comp. Neurol., 142:495–508.

    Article  Google Scholar 

  • Kanaseki, T., and Sprague, J.M., 1974, Anatomical organization of pretectal nuclei and tectal laminae in the cat. J. Comp. Neurol., 158:319–338.

    Article  Google Scholar 

  • Laemle, L.K., 1968, Retinal projections of Tupaia glis. Brain Behav. Evol., 1:473–499.

    Article  Google Scholar 

  • Laemle, L.K., and Noback, C.R., 1970, The visual pathways of the lorisid lemurs (Nycticebus coucang and Galago crassicaudatus). J. Comp. Neurol., 138:49–62.

    Article  Google Scholar 

  • Lane, R.H., Allman, J.M., and Kaas, J.H., 1971, Representation of the visual field in the superior colliculus of the grey squirrel (Sciurus carolinensis) and the tree shrew (Tupaia glis). Brain Res., 26:277–292.

    Google Scholar 

  • Lane, R.H., Allman, J.M., Kaas, J.H., and Miezin, F.M., 1973, The visuotopic organization of the superior colliculus of the owl monkey (Aotus trivirgatus) and the bushbaby (Galago senegalensis). Brain Res, 60:335–349.

    Article  Google Scholar 

  • Lane, R.H., Kaas, J.H., and Allman, J.M., 1974, Visuotopic organization of the superior colliculus in normal and Siamese cats. Brain Res., 70:413–430.

    Article  Google Scholar 

  • Le Gros Clark, W.E., 1962. The Antecedents of Man, University of Edinburgh Press, Edinburgh.

    Google Scholar 

  • Lund, J.S., Lund, R.D., Hendrickson, A.E., Bunt, A.H., and Fuchs, A.F., 1976, The origin of efferent pathways from the primary visual cortex, area 17, of the macaque monkey as shown by retrograde transport of horseradish peroxidase. J. Comp. Neurol., 164:287–304.

    Article  Google Scholar 

  • Martin, R.D., 1968, Towards a new definition of primates. Man, 3:377–401.

    Article  Google Scholar 

  • Martin, R.D., 1973, Comparative anatomy and primate systematics. Symp. Zool. Soc. London, 33:301–337.

    Google Scholar 

  • Martin, R.D., 1979. Phylogenetic aspects of prosimian behavior. In, The Study of Prosimian Behavior, G.A. Doyle and R.D. Martin, eds., Academic Press, New York.

    Google Scholar 

  • Meadows, J.C., 1974, The anatomical basis of prosopagnosia. J. Neurol. Neurosurg. Psychiatr., 37:489–501.

    Article  Google Scholar 

  • Merzenich, M.M., Kaas, J.H., Sur, M., and Lin, C.S., 1978, Double representation of the body surface within cytoarchitectonic areas 3b and 1 in SI in the owl monkey (Aotus trivirgatus). J. Comp. Neurol., 181:41–74.

    Article  Google Scholar 

  • Myerson, J., Manis, P.B., Miezin, F.M., and Allman, J.M., 1977, Magnification in striate cortex and retinal ganglion cell layer of owl monkey: a quantitative comparison. Science, 198:855.

    Article  Google Scholar 

  • Newsome, W.T., and Allman, J.M., 1980, The interhemispheric connections of visual cortex in the owl monkey, Aotus trivirgatus, and the bushbaby, Galago senegalensis. J. Comp. Neurol., 194:209–234.

    Article  Google Scholar 

  • Newsome, W.T., Maunsell, J.H.R., and Van Essen, D.C., 1980, Areal boundaries and topographic organization of the ventral posterior area (VP) of the macaque monkey. Soc. Neurosci. Abstr., 6:579.

    Google Scholar 

  • Palmer, L.A., Rosenquist, A.C., and Tusa, R.J., 1978, The retinotopic organization of lateral suprasylvian visual areas in the cat. J. Comp. Neurol., 177:237–256.

    Article  Google Scholar 

  • Pearson, L.J., Sanderson, K.J., and Wells, R.T., 1976, Retinal projections in the ringtailed possum Pseudocheirus peregrinus. J. Comp. Neurol., 170:227–240.

    Article  Google Scholar 

  • Penfield, W., and Roberts, L.A., 1959. Speech and Brain Mechanisms, Princeton Univ. Press, Princeton.

    Google Scholar 

  • Perrett, D.I., Rolls, E.T., and Caan, W., 1979, Temporal lobe cells of the monkey with visual responses selective for faces. Neurosci. Lett., 53:358.

    Google Scholar 

  • Petersen, S.E., Baker, J.F., and Allman, J.M., 1980, Dimensional selectivity of neurons in the dorsolateral visual area of the owl monkey. Brain Res., 197:507–511.

    Article  Google Scholar 

  • Polyak, S.D., 1957. The Vertebrate Visual System, Univ. of Chicago Press, Chicago.

    Google Scholar 

  • Radinsky, L.B., 1967, The oldest primate endocast. Am. J. Phys. Anthropol., 27:385–388.

    Article  Google Scholar 

  • Radinsky, L.B., 1970. The fossil evidence of prosimian brain evolution. In, The Primate Brain, C.R. Noback and W. Montagna, eds., Appleton-Century-Crofts, New York, pp. 209–224.

    Google Scholar 

  • Radinsky, L.B., 1977, Early primate brains: Facts and fiction. J. Hum. Evol., 6:79–86.

    Article  Google Scholar 

  • Rockel, A.J., Heath, C.J., and Jones, E.G., 1972, Afferent connections to the diencephalon in the marsupial phalanger and the question of sensory convergence in the “posterior group” of the thalamus. J. Comp. Neurol., 145:105–130.

    Article  Google Scholar 

  • Romer, A.S., 1966. Vertebrate Paleontology, 3rd ed., Univ. Chicago Press, Chicago.

    Google Scholar 

  • Sanghera, M.K., Rolls, E.T., and Roper-Hall, A., 1979, Visual responses of neurons in the dorsolateral amygdala of the alert monkey. Exp. Neurol., 63:610–626.

    Article  Google Scholar 

  • Sanides, F., 1970. Functional architecture of motor and sensory cortices in primates in light of a new concept of neocortical evolution. The Primate Brain, C.R. Noback and W. Montagna, eds., Appleton-Century-Crofts, New York, pp. 137–208.

    Google Scholar 

  • Schilling, A., 1979. Olfactory communication in prosimians. In, The Study of Prosimian Behavior, G.A. Doyle and R.D. Martin, eds., Academic Press, New York.

    Google Scholar 

  • Schwassmann, H.O., and Kruger, L., 1965, Organization of the visual projection upon the optic tectum of some fresh water fish. J. Comp. Neurol., 124:113–126.

    Article  Google Scholar 

  • Sebeok, T.A., 1977. How Animals Communicate, Indiana University Press, Bloomington.

    Google Scholar 

  • Siminoff, R., Schwassman, H.O., and Kruger, L., 1966, An electrophysiological study of the visual projection to the superior colliculus of the rat. J. Comp. Neurol., 127:435–444.

    Article  Google Scholar 

  • Spatz, W.B., 1975, An efferent connection of the solitary cells of Meynert. A study with horseradish peroxidase in the marmoset Callithrix. Brain Res., 92:450–455.

    Article  Google Scholar 

  • Spatz, W.B., and Tigges, J., 1972, Experimental-anatomical studies on the “Middle Temporal Visual Area (MT)” in primates. I. Efferent cortical connections in the marmoset (Callithrix jacchus). J. Comp. Neurol., 146:451–463.

    Article  Google Scholar 

  • Stephan, H., and Andy, O.J., 1970. The allocortex in primates. In, The Primate Brain, C.R. Noback and W. Montagna, eds., Appleton-Century-Crofts, New York, pp. 109–135.

    Google Scholar 

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

    Article  Google Scholar 

  • Tigges, J., 1966, Ein experimenteller Beitrag zum subkortikalen optischen System von Tupaia glis. Folia Primatologia, 4:103–123.

    Article  Google Scholar 

  • Tigges, J., 1970, Retinal projection to subcortical optic nuclei in diurnal and nocturnal squirrels. Brain Behav. Evol., 3:121–134.

    Article  Google Scholar 

  • Tigges, J., and O’Steen, W., 1974, Termination of retinofugal fibers in squirrel monkey: A re-investigation using autoradiographic methods. Brain Res., 79:489–495.

    Article  Google Scholar 

  • Tigges, J., Bos, J., and Tigges, M., 1977, An autoradiographic investigation of the subcortical visual system in chimpanzee. J. Comp. Neurol., 172:367–380.

    Article  Google Scholar 

  • Tigges, J., Tigges, M., and Kalaha, C.S., 1973, Efferent connections of area 17 in Galago. Am. J. Phys. Anthropol., 38:393–398.

    Article  Google Scholar 

  • Tigges, M., and Tigges, J., 1970, The retinofugal fibers and their terminal nuclei in Galago crassicaudatus (primates). J. Comp. Neurol., 138:87–102.

    Article  Google Scholar 

  • Turner, B.H., Mishkin, M., and Knapp, M., 1980, Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey. J. Comp. Neurol., 191:515–543.

    Article  Google Scholar 

  • Tusa, R.J., and Palmer, L.A., 1980. The retinotopic organization of area 20 and 21 in the cat. J. Comp. Neurol., in press.

    Google Scholar 

  • Ungerleider, L.G., and Mishkin, M., 1979, The striate projection zone in the superior temporal sulcus of Macaca mulatta: Location and topographic organization. J. Comp. Neurol., 188:347–366.

    Article  Google Scholar 

  • Updyke, B.V., 1974, Characteristics of unit responses in superior colliculus of the Cebus monkey. J. Neurophysiol., 37:896–909.

    Google Scholar 

  • Van Buren, J.M., 1963. The Retinal Ganglion Cell Layer, Charles C Thomas, Springfield.

    Google Scholar 

  • Van Essen, D.C., 1979. Visual cortical areas. In, Ann. Rev. Neurosci., W.M. Cowan, ed., Ann. Reviews, Inc., Palo Alto.

    Google Scholar 

  • Van Essen, D.C., and Zeki, S.M., 1978, The topographic organization of rhesus monkey prestriate cortex. J. Physiol. Lond., 277:193.

    Google Scholar 

  • Van Essen, D.C., Maunsell, J.H.R., and Bixby, J.L., 1980. The organization of extrastriate visual areas in the macaque monkey. In, Multiple Cortical Areas, C.N. Woolsey, ed., Humana Press, Englewood Cliffs, N.J., in press.

    Google Scholar 

  • Volchan, E., Rocha-Miranda, C.E., Lent, R., and Gawryszewski, L.G., 1978. The retinotopic organization of the superior colliculus in the opossum (Didelphis marsupialis aurita). In, Opossum Neurobiology, C.E. Rocha-Miranda and R. Lent, eds., Academia Brasileira de Ciencias, Rio de Janeiro.

    Google Scholar 

  • Weiler, R.E., and Kaas, J.H., 1980. Connections of the dorsolateral visual area (DL) of extrastriate visual cortex of the owl monkey (Aotus trivirgatus). Soc. Neurosci. Abstr., in press.

    Google Scholar 

  • Wilson, E.O., 1975. Sociobiology, Harvard University Press, Cambridge, Mass.

    Google Scholar 

  • Zeki, S.M., 1974, Functional organization of a visual area in the posterior bank of the superior temporal sulcus of the rhesus monkey. J. Physiol. Lond., 236:549.

    Google Scholar 

  • Zeki, S.M., 1980, The response properties of cells in the middle temporal area (area MT) of owl monkey visual cortex. Proc. Roy. Soc. Lond. B. 207:239.

    Article  Google Scholar 

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Allman, J. (1982). Reconstructing the Evolution of the Brain in Primates Through the Use of Comparative Neurophysiological and Neuroanatomical Data. In: Armstrong, E., Falk, D. (eds) Primate Brain Evolution. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-4148-2_2

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  • DOI: https://doi.org/10.1007/978-1-4684-4148-2_2

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