Skip to main content
Log in

Cortical heterogeneity: Implications for visual processing and polysensory integration

  • Published:
Journal of Neurocytology

Abstract

Recent studies have revealed substantial variation in pyramidal cell structure in different cortical areas. Moreover, cell morphology has been shown to vary in a systematic fashion such that cells in visual association areas are larger and more spinous than those in the primary visual area. Various aspects of these structural differences appear to be important in influencing neuronal function. At the cellular level, differences in the branching patterns in the dendritic arbour may allow for varying degrees of non-linear compartmentalisation. Differences in total dendritic length and spine number may determine the number of inputs integrated by individual cells. Variations in spine density and geometry may affect cooperativity of inputs and shunting inhibition, and the tangential dimension of the dendritic arbours may determine sampling strategies within cortex. At the systems level, regional variation in pyramidal cell structure may determine thedegree of recurrent excitation through reentrant circuits influencing the discharge properties of individual neurones and the functional signature of the circuits they compose. The ability of pyramidal neurones in visual areas of the parietal and temporal lobes to integrate large numbers of excitatory inputs may also facilitate cortical binding. Here I summarise what I consider to be among the most salient, and testable, aspects of an inter-relationship between morphological and functional heterogeneity in visual cortex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson, J. C., Binzegger, T., Martin, K. A. C. &; Rockland, K. S. (1998) The connection from cortical area V1 to V5: A light and electron microscopic study. Journal of Neuroscience 18, 10525–10540.

    PubMed  Google Scholar 

  • Angelucci, A., Levitt, J. B., Walton, E. J., Hupe, J. M., Bullier, J. &; Lund, J. S. (2002) Circuits for local and global signal integration in primary visual cortex. Journal of Neuroscience 22, 8633–8646.

    PubMed  Google Scholar 

  • Angelucci, A., Levitt, J. B. &; Lund, J. S. (2002) Anatomical origins of the classical receptive field and modulatory surround field of single neurons in macaque visual cortical area V1. In Prog. Brain. Res. (edited by Azmitia, E., deFelipe, J., Jones, E. G., Rakic, P. &; Ribak, C. E.) pp. 371–388. Amsterdam: Elsevier.

    Google Scholar 

  • Ashford, J. W. &; Fuster, J. M. (1985) Occipital and inferotemporal responses to visual signals in the monkey. Experimental Neurology 90, 444–446.

    PubMed  Google Scholar 

  • Beaulieu, C. &; Somogyi, P. (1990) Targets and quantitative distribution of GABAergic synapses in the visual cortex of the cat. European Journal of Neuroscience 2, 296–303.

    PubMed  Google Scholar 

  • Beaulieu, C., KisvÁrday, Z., Somogyi, P., Cynader, M. &; Cowey, A. (1992) Quantitative distribution of GABA-immunopositive and-immunonegative neurons and synapses in the monkey striate cortex (area 17). Cerebral Cortex 2, 295–309.

    PubMed  Google Scholar 

  • Beaulieu, C. &; Colonnier, M. (1985) A laminar analysis of the number of round-asymmetrical and flatsymmetrical synapses on spines, dendritic trunks, and cell bodies in area 17 of the cat. Journal of Comparative Neurology 231, 180–189.

    PubMed  Google Scholar 

  • Boussaoud, D., Desimone, R. &; Ungerleider, L. G. (1991) Visual topography of area TEO in the macaque. Journal of Comparative Neurology 306, 554–575.

    PubMed  Google Scholar 

  • Brodmann, K. (1907) Beiträge zur histologischen lokalisation der großhirnrinde. Journal of Psychology and Neurology 6, 1–16.

    Google Scholar 

  • Bullier, J., Girard, P. &; Salin, P. A. (1994) The role of area 17 in the transfer of information to extrastriate visual cortex. In Cerebral Cortex Vol. 10, Primary Visual Cortex in Primates (edited by Peters, A. &; Rockland, K. S.) pp. 301–331. New York: Plenum.

    Google Scholar 

  • Calford, M. B. (2002) Dynamic representational plasticity in sensory cortex. Neuroscience 111, 709–738.

    PubMed  Google Scholar 

  • Calvin, W. H. &; Sypert, G. W. (1976) Fast and slow tract pyramidal neurons:Anintracellular analysis of their contrasting firing properties in the cat. Journal of Neurophysiology 39, 420–434.

    PubMed  Google Scholar 

  • Casagrande, V. A. &; Kaas, J. H. (1994) The afferent, intrinsic and efferent connections of primary visual cortex in primates. In Cerebral Cortex Vol. 10, Primary Visual Cortex in Primates (edited by Peters, A. &; Rockland, K. S.) pp. 201–259. New York: Plenum.

    Google Scholar 

  • Chagnac-Amitai, Y., Luhmann, H. J. &; Prince, D. A. (1990) Burst generating and regular spiking layer V pyramidal neurons of rat neocortex have different morphological features. Journal of Comparative Neurology 296, 598–613.

    PubMed  Google Scholar 

  • Colonnier, M. (1968) Synaptic patterns on different cell types in the different laminae of the cat visual cortex. Brain Research 9, 268–287.

    PubMed  Google Scholar 

  • Colonnier, M. &; Rosignol, S. (1969) Heterogeneity of the cerebral cortex. In Basic Mechanisms of the Epilepsies (edited by Jasper, H., Ward, A. &; Pope, A.) pp. 29–40. Boston: Little Brown.

    Google Scholar 

  • Conway, B. R., Hubel, D. H. &; Livingstone, M. S. (2002) Color contrast in macaque V1. Cerebral Cortex 12, 915–925.

    PubMed  Google Scholar 

  • Cowey, A. &; Stoerig, P. (1991) The neurobiology of blindsight. Trends in Neuroscience 14, 140–145.

    Google Scholar 

  • Creutzfeldt, O. D. (1977) Generality of the functional structure of the neocortex. Naturwissenschaften 64, 507–517.

    PubMed  Google Scholar 

  • Cusick, C. G., Seltzer, B., Cola, M. &; Griggs, E. (1995) Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex. Journal of Comparative Neurology 360, 513–535.

    PubMed  Google Scholar 

  • dela PeÑa, E. &; Geijo-Barrientos, E. (1996) Laminar localization, morphology, and physiological properties of pyramidal neurons that have low-threshold calcium current in the guinea pig medial frontal cortex. Journal of Neuroscience 16, 5301–5311.

    PubMed  Google Scholar 

  • de Lima, A. D., Voigt, T. &; Morrison, J. H. (1990) Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. Journal of Comparative Neurology 296, 159–172.

    PubMed  Google Scholar 

  • deFelipe, J. (1997) Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. Journal of Chemical Neuroanatomy 14, 1–19.

    PubMed  Google Scholar 

  • deFelipe, J. &; FariÑas, I. (1992) The pyramidal neuron of the cerebral cortex: Morphological and chemical characteristics of the synaptic inputs. Progress in Neurobiology 39, 563–607.

    PubMed  Google Scholar 

  • deFelipe, J. &; Jones, E. G. (1985) Vertical organization of γ-aminobutyric acid-accumulating intrinsic neuronal systems in monkey cerebral cortex. Journal of Neuroscience 5, 3246–3260.

    PubMed  Google Scholar 

  • deFelipe, J., Conti, F., van Eyck, S. L. &; Manzoni, T. (1988) Demonstration of glutamatepositive axon terminals forming asymmetric synapses in cat neocortex. Brain Research 455, 162–165.

    PubMed  Google Scholar 

  • deFelipe, J., del RÍo, M. R., GonzÁlez-Albo, M. C. &; Elston, G. N. (1999) Distribution and patterns of connectivity of interneurons containing calbindin, calretinin and parvalbumin in visual areas of the occipital and temporal lobes of the macaque monkey. Journal of Comparative Neurology 412, 515–526.

    Google Scholar 

  • Deschenes, M., Labelle, A. &; Landry, P. (1979) Morphological characterization of slow and fast pyramidal tract cells in the cat. Brain Research 178, 251–274.

    PubMed  Google Scholar 

  • Douglas, R. J., Martin, K. A. C. &; Whitteridge, D. (1989) A canonical microcircuit for neocortex. Neural Computation 1, 480–488.

    Google Scholar 

  • Douglas, R. J. &; Martin, K. A. C. (1998) The synaptic organization of the brain. In Neocortex (edited by Shepherd, G. M.) pp. 735–769. New York: Oxford University Press.

    Google Scholar 

  • Eccles, J. C. (1984) The cerebral neocortex: A theory of its operation. In Cerebral Cortex Vol. 1, Cellular Components of the Cerebral Cortex (edited by Peters, A. &; Jones, E. G.) pp. 1–32. New York: Plenum.

    Google Scholar 

  • Elston, G. N. (2000) Pyramidal cells of the frontal lobe: All the more spinous to think with. Journal of Neuroscience 20, RC95(1-4).

  • Elston, G. N. (2001) Interlaminar differences in the pyramidal cell phenotype in cortical areas 7m and STP of the macaque monkey. Experimental Brain Research 138, 141–152.

    Google Scholar 

  • Elston, G. N. (2003a) Comparative studies of pyramidal neurons in visual cortex of monkeys. In The Primate Visual System (edited by Kaas, J. H. &; Collins, C.) pp. 365–385. Boca Raton: CRC.

    Google Scholar 

  • Elston, G. N. (2003b) Cortex, cognition and the cell: New insights into the pyramidal cell and prefrontal function. Cerebral Cortex.

  • Elston, G. N. (2003c) Pyramidal cell heterogeneity in the visual cortex of the nocturnal New World owl monkey (Aotus trivirgatus). Neuroscience 117, 213–219.

    PubMed  Google Scholar 

  • Elston, G. N. (2003d) The pyramidal neuron in occipital, temporal and prefrontal cortex of the owl monkey (Aotus trivirgatus): Regional specializatoin in cell structure. European Journal of Neuroscience 17, 1313–1318.

    PubMed  Google Scholar 

  • Elston, G. N. &; deFelipe, J. (2002) Spine distribution in neocortical pyramidal cells: A common organizational principle. In Progress in Brain Research (edited by Azmitia, E. C., deFelipe, J., Jones, E. G., Rakic, P. &; Ribak, C. E.) pp. 109–133. Amsterdam: Elsevier.

    Google Scholar 

  • Elston, G. N. &; GonzÁlez-Albo, M. C. (2003) Density and distribution of parvalbumin-, calbindin-, and calretinin-immunoreactive neurons in the prefrontal cortex of the owl monkey (Aotus trivirgatus): A quantitative comparison with sensory and motor cortical areas. Brain, Behavior and Evolution, in press.

  • Elston, G. N. &; Jelinek, H. F. (2001) Dendritic branching patterns of pyramidal cells in the visual cortex of the New World marmoset monkey, with comparative notes on the Old World macaque monkey. Fractals 9, 297–303.

    Google Scholar 

  • Elston, G. N. &; Rockland, K. (2002) The pyramidal cell in sensory-motor cortex of the macaque monkey: Phenotypic variation. Cerebral Cortex 12, 1071–1078.

    PubMed  Google Scholar 

  • Elston, G. N. &; Rosa, M. G. P. (1997) The occipitoparietal pathway of the macaque monkey: Comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cerebral Cortex 7, 432–452.

    PubMed  Google Scholar 

  • Elston, G. N. &; Rosa, M. G. P. (1998a) Complex dendritic fields of pyramidal cells in the frontal eye field of the macaque monkey: Comparison with parietal areas 7a and LIP. NeuroReport 9, 127–131.

    PubMed  Google Scholar 

  • Elston, G. N. &; Rosa, M. G. P. (1998b) Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cerebral Cortex 8, 278–294.

    PubMed  Google Scholar 

  • Elston, G. N. &; Rosa, M. G. P. (2000) Pyramidal cells, patches, and cortical columns: A comparative study of infragranular neurons in TEO, TE, and the superior temporal polysensory area of the macaque monkey. Journal of Neuroscience 20, RC117 (1-5).

  • Elston, G. N., Benavides-Piccione, R. &; deFelipe, J. (2001) The pyramidal cell in cognition: A comparative study in human and monkey. Journal of Neuroscience 21, RC163(1-5)

  • Elston, G. N., deFelipe, J., Arellano, J. I., GonzÁlez-Albo, M. C. &; Rosa, M. G. P. (1999c) Variation in the spatial relationship between parvalbumin immunoreactive interneurones and pyramidal neurones in rat somatosensory cortex. NeuroReport 10, 2975–2979.

    PubMed  Google Scholar 

  • Elston, G. N., Rosa, M. G. P. &; Calford, M. B. (1996) Comparison of dendritic fields of layer III pyramidal neurones in striate and extrastriate visual areas of the marmoset: A Lucifer Yellow intracellular injection study. Cerebral Cortex 6, 807–813.

    PubMed  Google Scholar 

  • Elston, G. N., Tweedale, R. &; Rosa, M. G. P. (1999a) Cortical integration in the visual system of the macaque monkey: Large scale morphological differences of pyramidal neurones in the occipital, parietal and temporal lobes. Proceedings of the Royal Society Series B 266, 1367–1374.

    Google Scholar 

  • Elston, G. N., Tweedale, R. &; Rosa, M. G. P. (1999b) Cellular heterogeneity in cerebral cortex. A study of the morphology of pyramidal neurones in visual areas of the marmoset monkey. Journal of Comparative Neurology 415, 33–51.

    PubMed  Google Scholar 

  • Feldman, D. (1984) Morphology of the neocortical pyramidal neuron. In Cerebral Cortex Vol. 1, Cellular Components of the Cerebral Cortex (edited by Peters, A. &; Jones, E. G.) pp. 123–200. New York: Plenum.

    Google Scholar 

  • Felleman, D. J. &; van Essen, D. C. (1991) Distributed hierarchical processing in primate cerebral cortex. Cerebral Cortex 1, 1–47.

    PubMed  Google Scholar 

  • Ferster, D. &; Miller, K. D. (2000) Neural mechanisms of orientation selectivity in the visual cortex. Annual Review of Neuroscience 23, 441–71.

    PubMed  Google Scholar 

  • Friston, K. J. (2001) Brain function, nonlinear coupling, and neuronal transients. Neuroscientist 7, 406–418.

    PubMed  Google Scholar 

  • Fujita, I. (1997) The inferior temporal cortex; columns and horizontal axons. In The Association Cortex, Structure and Function (edited by Sakata, H., Mikami, A. &; Fuster, J.) pp. 247–258. Amsterdam: Harwood Academic Publishers.

    Google Scholar 

  • Fujita, I. &; Fujita, T. (1996) Intrinsic connections in the macaque inferior temporal cortex. Journal of Comparative Neurology 368, 467–486.

    PubMed  Google Scholar 

  • Fuster, J. M. (2000) Cortical dynamics of memory. International Journal of Psychophysiology 35, 155–164.

    PubMed  Google Scholar 

  • Garey, L. J., Dreher, B. &; Robinson, S. R. (1991) The organization of the visual thalamus. In Neuroanatomy of the Visual Pathways and their Development (edited by Dreher, B. &; Robinson, S. R.) pp. 176–234. London: MacMillan Press.

    Google Scholar 

  • Gilbert, C. D. (1993) Circuitry, architecture, and functional dynamics of visual cortex. Cerebral Cortex 3, 373–386.

    PubMed  Google Scholar 

  • Gilbert, C. D. (1998) Adult cortical dynamics. Physiological Reviews 78, 467–485.

    PubMed  Google Scholar 

  • Gilbert, C. D. &; Wiesel, T. N. (1979) Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex. Nature 280, 120–125.

    PubMed  Google Scholar 

  • Gilbert, C. D. &; Wiesel, T. N. (1983) Clustered intrinsic connections in cat visual cortex. Journal of Neuroscience 3, 1116–1133.

    PubMed  Google Scholar 

  • Gilbert, C. D. &; Wiesel, T. N. (1989) Columnar specificity of intrinsic horizontal and corticocortical connections in the cat visual cortex. Journal of Neuroscience 9, 2432–2442.

    PubMed  Google Scholar 

  • Gross, C. G. &; Bender, D. B. (1969) Visual receptive fields of neurones in inferotemporal cortex of the monkey. Science 166, 1303–1306.

    PubMed  Google Scholar 

  • Gross, C. G., Rodman, H. R., Gochin, P. M. &; Colombo, M. W. (1993) Inferior temporal cortex as a pattern recognition device. In Computational Learning and Recognition: Proceedings of the 3rd NEC Research Symposium (edited by Baum, E.) pp. 44–73. Philadelphia: Society for Industrial and Applied Mathematics.

    Google Scholar 

  • Hamada, I., Sakai, M. &; Kubota, K. (1981) Morphological differences between fast and slow pyramidal tract neurons in the monkey motor cortex as revealed by intracellular injections of horseradish peroxidase by pressure. Neuroscience Letters 22, 233–238.

    Google Scholar 

  • Haug, H. (1987). Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: A stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores and one elephant). American Journal of Anatomy 180, 126–142.

    PubMed  Google Scholar 

  • Hendry, S. H. C. &; Calkins, D. J. (1998) Neuronal chemistry and functional organization in the primate visual system. Trends in Neuroscience 21, 344–349.

    Google Scholar 

  • Hendry, S. H. C., Schwark, H. D., Jones, E. G. &; Yan, J. (1987) Numbers and proportions of GABA-immunoreactive neurons in different areas of monkey cerebral cortex. Journal of Neuroscience 7, 1503–1519.

    PubMed  Google Scholar 

  • Hikosaka, K. (1999) Tolerance of responses to visual patterns in neurons of the posterior inferotemporal cortex in the macaque against changing stimulus size and orientation, and deleting patterns. Behavioural Brain Research 100, 67–76.

    PubMed  Google Scholar 

  • Hikosaka, K., Iwai, E., Saito, H. &; Tanaka, K. (1988) Polysensory properties of neurones in the anterior bank of the caudal superior temporal sulcus of the macaque monkey. Journal of Neurophysiology 60, 1615–1637.

    PubMed  Google Scholar 

  • Hof, P. R. &; Morrison, J. H. (1995) Neurofilament protein defines regional patterns of cortical organization in the macaque monkey visual system: A quantitative immunohistochemical analysis. Journal of Comparative Neurology 352, 161–186.

    PubMed  Google Scholar 

  • Hof, P. R., Glezer, I. I., CondÉ, F., Flagg, R. A., Rubin, M. B., Nimchinsky, E. A. &; Vogt Wiesenhorn, D. M. (1999) Cellular distribution of the calcium-binding proteins parvalbumin, calbindin and calretinin in the neocortex of mammals: Phylogenetic and developmental patterns. Journal of Chemical Neuroanatomy 16, 77–116.

    PubMed  Google Scholar 

  • Houser, C. R., Vaughn, J. E., Hendry, S. H. C., Jones, E. G. &; Peters, A. (1984) GABA neurons in cerebral cortex. In Cerebral Cortex Vol. 2, Functional Properties of Cortical Cells (edited by Jones, E. G. &; Peters, A.) pp. 63–89. New York: Plenum.

    Google Scholar 

  • Hubel, D. H. &; Livingstone, M. S. (1987) Segregation of form, color, and stereopsis in primate area 18. Journal of Neuroscience 7, 3378–3415.

    PubMed  Google Scholar 

  • Innocenti, G. M. (1986) General organization of callosal connections in the cerebral cortex. In Cerebral Cortex Vol. 5, Sensory-Motor Areas and Aspects of Cortical Connectivity (edited by Jones, E. G. &; Peters, A.) pp. 291–353. New York: Plenum.

    Google Scholar 

  • Jacobs, B. &; Scheibel, A. B. (2002) Regional dendritic variation in primate cortical pyramidal cells. In Cortical Areas: Unity and Diversity (edited by SchÜz, A. &; Miller, R.) pp. 111–131. London: Taylor and Francis.

    Google Scholar 

  • Jacobs, B., Schall, M., Prather, M., Kapler, L., Driscoll, L., Baca, S., Jacobs, J., Ford, K., Wainwright, M. &; Treml, M. (2001) Regional dendritic and spine variation in human cerebral cortex: A quantitative study. Cerebral Cortex 11, 558–571.

    PubMed  Google Scholar 

  • Jelinek, H. F. &; Elston, G. N. (2001) Pyramidal neurones in macaque visual cortex: Interareal phenotypic variation of dendritic branching patterns. Fractals 9, 287–295.

    Google Scholar 

  • Johnson, R. R. &; Burkhalter, A. (1996) Microcircuitry of forward and feedback connections within rat visual cortex. Journal of Comparative Neurology 368, 383–398.

    PubMed  Google Scholar 

  • Jones, E. G. (1968) An electron microscopic study of the terminations of afferent fiber systems onto the somatic sensory cortex of the cat. Journal of Anatomy 103, 595–597.

    Google Scholar 

  • Jones, E. G. (1981) Anatomy of cerebral cortex: Columnar input-output organization. In The Cerebral Cortex (edited by Schmitt, F. O., Worden, F. G., Adelman, G. &; Dennis, M.) pp. 199–235. Cambridge, MA: MIT Press.

    Google Scholar 

  • Jones, E. G. (1983) The columnar basis of cortical circuitry. In The Clinical Neurosciences (edited by Willis, W. D.) pp. 357–383. New York: Churchill Livingstone.

    Google Scholar 

  • Jones, E. G. (1984) Laminar distribution of cortical efferent cells. In Cerebral Cortex Vol. 1, Cellular Components of the Cerebral Cortex (edited by Peters, A. &; Jones, E. G.) pp. 521–553. New York: Plenum.

    Google Scholar 

  • Jones, E. G. (1993) GABAergic neurons and their role in cortical plasticity in primates. Cerebral Cortex 3, 361–372.

    PubMed  Google Scholar 

  • Kaas, J. H. (1982) The segregation of function in the nervous system: Why do sensory systems have so many subdivisions? In Contributions to Sensory Physiology (edited by Neff, W. P.) pp. 201–240. New York: Academic Press.

    Google Scholar 

  • Kaas, J. H. (1984) The organization of sensory and motor cortex in owl monkeys. In Aotus: The Owl Monkey (edited by Baer, J. F., Weller, R. E. &; Kakoma, I.) pp. 331–351. Orlando: Academic Press.

    Google Scholar 

  • Kaas, J. H. (1986) The structural basis for information processing in the primate visual system. In Visual Neuroscience (edited by Pettigrew, J. P., Sanderson, K. J. &; Levick, W. R.) pp. 315–339. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Kaas, J. H. (1987) The organization of neocortex in mammals: Implications for theories of brain function. Annual Reviews in Psychology 38, 129–151.

    Google Scholar 

  • Kaas, J. H. (1989a) The evolution of complex sensory systems in mammals. Journal of Experimental Biology 146, 165–176.

    PubMed  Google Scholar 

  • Kaas, J. H. (1989b) Why does the brain have so many visual areas? Journal of Cognitive Neuroscience 1, 121–135.

    Google Scholar 

  • Kaas, J. H. (1991) Plasticity of sensory and motor maps in adult mammals. Annual Reviews of Neuroscience 14, 137–167.

    Google Scholar 

  • Kaas, J. H. (1995) The evolution of isocortex. Brain Behavior and Evolution 46, 187–196.

    Google Scholar 

  • Kharazia, V. N., Weinberg, R. J. (1993) Glutamate in terminals of the thalamocortical fibers in rat somatic sensory cortex. Neuroscience Letters 157, 162–166.

    PubMed  Google Scholar 

  • KisvÁrday, Z. F. &; Eysel, U. T. (1992) Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 46, 275–286.

    PubMed  Google Scholar 

  • KisÁrday, Z. F., Beaulieu, C. &; Eysel, U. T. (1993) Network of GABAergic large basket cells in cat visual cortex (area 18): Implications for lateral disinhibition. Journal of Comparative Neurology 327, 398–415.

    PubMed  Google Scholar 

  • KisvÁrday, Z. F., Martin, K. A. C., Freund, T. F., Magloczky, Z., Whitteridge, D. &; Somogyi, P. (1986) Synaptic targets of HRP-filled layer III pyramidal cells in the cat striate cortex. Experimental Brain Research 64, 541–552.

    Google Scholar 

  • Koch, C. (1999) Biophysics of Computation. Information Processing in Single Neurons. New York: Oxford University Press.

    Google Scholar 

  • Koch, C., Poggio, T. &; Torre, V. (1982) Retinal ganglion cells: A functional interpretation of dendritic morphology. Philosophical Transactions of the Royal Society of London Series B 298, 227–264.

    PubMed  Google Scholar 

  • Kolb, B. &; Tees, R. C. (1990) The rat as a model of cortical function. In The Cerebral Cortex of the Rat (edited by Kolb, B. &; Tees, R. C.) pp. 3–17. Cambridge, MA: MIT Press.

    Google Scholar 

  • Kondo, H. T., Tanaka, K., Hashikawa, T. &; Jones, E. G. (1999) Neurochemical gradients along monkey sensory cortical pathways: Calbindinimmunoreactive pyramidal neurons in layers II and III. European Journal of Neuroscience 11, 4197–4203.

    PubMed  Google Scholar 

  • Kritzer, M. &; Goldman-Rakic, P. S. (1995) Intrinsic circuit organization of the major layers and sublayers of the dorsolateral prefrontal cortex in monkeys. Journal of Comparative Neurology 359, 131–143.

    PubMed  Google Scholar 

  • Kritzer, M., Cowey, A. &; Somogyi, P. (1992) Patterns of inter-and intralaminar GABAergic connections distinguish striate (V1) and extrastriate (V2, V4) visual cortices and their functionally specialized subdivisions in the rhesus monkeys. Journal of Neuroscience 12, 4545–4564.

    PubMed  Google Scholar 

  • Krubitzer, L. A. (1995) The organization of neocortex in mammals: Are species differences really so different? Trends in Neuroscience 18, 408–417.

    Google Scholar 

  • Krubitzer, L. A. (2000) How does evolution build a complex brain. In Evolutionary Developmental Biology of the Cerebral Cortex (edited by Bock G. R. &; Carden, G.) pp. 206–226. Chichester: Wiley.

    Google Scholar 

  • Larkman, A. U. (1991) Dendritic morphology of pyramidal neurones in the visual cortex of the rat: III. Spine distributions. Journal of Comparative Neurology 306, 332–343.

    PubMed  Google Scholar 

  • Lennie, P. (1998) Single units and visual cortical organization. Perception 27, 889–935.

    PubMed  Google Scholar 

  • Livingstone, M. S. (1998) Mechanisms of direction selectivity in macaque V1. Neuron 20, 509–526.

    PubMed  Google Scholar 

  • Livingstone, M. S. &; Hubel, D. H. (1984) Anatomy and physiology of a color system in the primate visual cortex. Journal of Neuroscience 4, 309–356.

    PubMed  Google Scholar 

  • LlinÁs, R. &; ParÉ, D. (1996) The brain as a closed system modulated by the senses. In The Mind Brain Continuum (edited by LlinÁs, R. &; Churchland, P. S.) pp. 1–18. Cambridge, MA: MIT Press.

    Google Scholar 

  • Lueschow, A., Miller, E. K. &; Desimone, R. (1994) Inferior temporal mechanisms for invariant object recognition. Cerebral Cortex 4, 523–531.

    PubMed  Google Scholar 

  • Lund, J. S., Yoshioka, T. &; Levitt, J. B. (1993) Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. Cerebral Cortex 3, 148–162.

    PubMed  Google Scholar 

  • Lund, J. S., Wu, Q., Hadingham, P. T., Levitt, J. B. (1995) Cells and circuits contributing to functional properties in area V1 of macaque monkey cerebral cortex: Bases for neuroanatomically realistic models. Journal of Anatomy 187, 563–581.

    PubMed  Google Scholar 

  • Lund, J. S., Hendrickson, A. E., Ogren, M. P. &; Tobin, E. A. (1981) Anatomical organization of primate visual cortex area VII. Journal of Comparative Neurology 202, 19–45.

    PubMed  Google Scholar 

  • Lyon, D. C. &; Kaas, J. H. (2001) Connectional and architectonic evidence for dorsal and ventral V3, and dorsomedial area in marmoset monkeys. Journal of Neuroscience 21, 249–261.

    PubMed  Google Scholar 

  • Lyon, D. C. &; Kaas, J. H. (2002) Evidence from connectional for both dorsal and ventral subdivisions of V3 in three species of monkeys. Journal of Comparative Neurology 449, 281–297.

    PubMed  Google Scholar 

  • Mainen, Z. F. &; Sejnowski, T. J. (1996) Influence of dendritic structure on firing pattern in model neocortical neurons. Nature 382, 363–366.

    PubMed  Google Scholar 

  • Malach, R. (1994) Cortical columns as devices for maximizing neuronal diversity. Trends in Neuroscience 17, 101–104.

    Google Scholar 

  • Malach, R., Amir, Y., Harel, M. &; Grinvald, A. (1993) Relationship between intrinsic connections and functional architecture revealed by optical imaging and in vivo targeted biocytin injections in primate striate cortex. Proceedings of the National Academy of Science USA 90, 10469–10473.

    Google Scholar 

  • Malonek, D., Tootell, R. B. H. &; Grinvald, A. (1994) Optical imaging reveals the functional architecture of neurons processing shape and motion in owl monkey area MT. Proceedings of the Royal Society Series B 258, 109–119.

    Google Scholar 

  • Martin, K. A. C. &; Whitteridge, D. (1984) Form, function and intracortical projections of spiny neurones in the striate visual cortex of the cat. Journal of Physiology (London) 353, 463–504.

    Google Scholar 

  • Mason, A. &; Larkman, A. U. (1990) Correlations between morphology and electrophysiology of pyramidal neurons in slices of rat visual cortex. II. Electrophysiology. Journal of Neuroscience 10, 1415–1428.

    PubMed  Google Scholar 

  • Matsubara, J., Cynader, M., Swindale, N. V. &; Stryker, M. P. (1985) Intrinsic projections within visual cortex: Evidence for orientation-specific local connections. Proceedings of the National Academy of Science USA 82, 935–939.

    Google Scholar 

  • McGuire, B. A., Gilbert, C. D., Rivlin, P. K. &; Wiesel, T. N. (1991) Targets of horizontal connections in macaque primary visual cortex. Journal of Comparative Neurology 305, 370–392.

    PubMed  Google Scholar 

  • Mel, B. (1992) NMDA-based pattern discrimination in a modelled cortical neuron. Neural Computation 4, 502–517.

    Google Scholar 

  • Mel, B. (1993) Synaptic integration in an excitable dendritic tree. Journal of Neurophysiology 70, 1086–1101.

    PubMed  Google Scholar 

  • Mel, B. (1999) Why have dendrites? A computational perspective. In Dendrites (edited by Stuart, G.,Spruston, N. & Äusser, M.H) pp.271-289. New York: Oxford University Press.

    Google Scholar 

  • Miller, E. K., Cohen, J. D. (2001) An integrative theory of prefrontal cortex. Annual Review of Neuroscience 24, 167–202.

    PubMed  Google Scholar 

  • Miller, E. K., Li, L. &; Desimone, R. (1993) Activity of neurons in anterior inferior temporal cortex during a short-term memory task. Journal of Neuroscience 13, 1460–1478.

    PubMed  Google Scholar 

  • Mitchison, G. &; Crick, F. H. C. (1982) Long axons within the striate cortex: Their distribution, orientation and patterns of connection. Proceedings of the National Academy of Science USA 79, 3661–3665.

    Google Scholar 

  • Morrison, J. H., Hof, P. R. &; Huntley, G. W. (1998) Neurochemical organization of the primate visual cortex. In Handbook of Chemical Neuroanatomy (edited by Bloom, F. F., BjÖrklund, A. &; HÖkfelt, T.) pp. 299–433. Amsterdam: Elsevier.

    Google Scholar 

  • Motter, B. C., Steinmetz, M. A., Duffy, C. J. &; Mountcastle, V. B. (1987) Functional properties of parietal visual neurons: Mechanisms of directionality along a single axis. Journal of Neuroscience 7, 154–176.

    PubMed  Google Scholar 

  • Mountcastle, V. B. (1978) An organizing principle for general cortical function: The unit module and the distributed system. In The Mindful Brain (edited by Schmitt, F. O.) pp. 7–50. Cambridge: MIT Press.

    Google Scholar 

  • Mountcastle, V. B. (1995) The evolution of ideas concerning the function of neocortex. Cerebral Cortex 5, 289–295.

    PubMed  Google Scholar 

  • Mountcastle, V. B. (1997) The columnar organization of the neocortex. Brain 120, 701–722.

    PubMed  Google Scholar 

  • Mountcastle, V. B. (1998) The Cerebral Cortex. Cambridge: Harvard University Press.

    Google Scholar 

  • Murayama, Y., Fujita, I. &; Kato, M. (1997) Contrasting forms of synaptic plasticity in monkey inferotemporal and primary visual cortices. NeuroReport 8, 1503–1508.

    PubMed  Google Scholar 

  • Nakamura, K. &; Kubota, K. (1995) Mnemonic firing of neurons in the monkey temporal pole during a visual recognition memory task. Journal of Neurophysiology 74, 162–178.

    PubMed  Google Scholar 

  • Nelson, R. B., Friedman, D. P., O'neill, J. B., Mishkin, M. &; Routtenberg, A. (1987) Gradients of protein kinase C substrate phosphorylation in primate visual system in visual memory storage areas. Brain Research 416, 387–392.

    PubMed  Google Scholar 

  • Northcutt, R. G. &; Kaas, J. H. (1995) The emergence and evolution of the mammalain neocortex. Trends in Neuroscience 18, 373–379.

    PubMed  Google Scholar 

  • Perrett, D. I., Smith, P. A. J., Potter, D. D., Mistlin, A. J., Head, A. S., Milner, A. D. &; Jeeves, M. A. (1984) Neurons responsive to faces in the temporal cortex: Studies of functional organization, sensitivity to identity and relation to perception. Human Neurobiology 3, 197–208.

    PubMed  Google Scholar 

  • Peters, A. &; Kaiserman-Abramof, I. A. (1969) The small pyramidal neuron of the rat cerebral cortex. The synapses upon dendritic spines. Zeitschrift für Zellforschung 100, 487–586.

    Google Scholar 

  • Peters, A. &; Harriman, K. M. (1992) Different kinds of axon terminals forming symmetric synapses with the cell bodies and initial axon segments of layer II/III pyramidal cells. III. Origins and frequency of occurence of the terminals. Journal of Neurocytology 21, 679–692.

    PubMed  Google Scholar 

  • Poirazi, P. &; Mel, B. (2001) Impact of active dendrites and structural plasticity on the storage capacity of neural tissue. Neuron 29, 779–796.

    PubMed  Google Scholar 

  • Preuss, T. M. (2001) The discovery of cerebral diversity: An unwelcome scientific revolution. In Evolutionary Anatomy of the Primate Cerebral Cortex (edited by Falk, D. &; Gibson, K. R.) pp. 138–164. Cambridge, UK: Cambridge University Press.

    Google Scholar 

  • Rall, W. (1959) Branching dendritic trees and motorneuron membrane resistivity. Experimental Neurology 1, 491–527.

    PubMed  Google Scholar 

  • Rall, W. (1964) Theoretical significance of dendritic tree for input-output relation. In Neural Theory and Modeling (edited by Reiss, R. F.) pp. 73–97. Stanford: Stanford University Press.

    Google Scholar 

  • Rall, W., Burke, R. E., Holmes, W. R., Jack, J. J. B., Redman, S. R. &; Segev, I. (1992) Matching dendritic neuron models to experimental data. Physiological Reviews 72, 159–186.

    Google Scholar 

  • Redman, S. &; Walmsley, B. (1983) The time course of synaptic potentials evoked in cat spinal motoneurones at identified group Ia synapses. Journal of Physiology 343, 117–133.

    PubMed  Google Scholar 

  • Rempel-Clower, N. L. &; Barbas, H. (2000) The laminar pattern of connections between prefrontal and anterior temporal corticies in the rhesus monkey is related to cortical structure and function. Cerebral Cortex 10, 851–865.

    PubMed  Google Scholar 

  • Ringo, J. L. (1991) Neuronal interconnection as a function of brain size. Brain, Behavior and Evolution 38, 1–6.

    Google Scholar 

  • Rockel, A. J., Hiorns, R. W. &; Powell, T. P. S. (1980) The basic uniformity in structure of the neocortex. Brain 103, 221–244.

    PubMed  Google Scholar 

  • Rockland, K. S. (1985)Areticular pattern of intrinsic connections in primate area V2 (area 18). Journal of Comparative Neurology 235, 467–478.

    PubMed  Google Scholar 

  • Rockland, K. S. (1989) Bistratified distribution of terminal arbors of individual axons projecting from area V1 to middle temporal area (MT) in the macaque monkey. Visual Neuroscience 3, 155–170.

    PubMed  Google Scholar 

  • Rockland, K. S. (1992) Configuration, in serial reconstruction, of individual axons projecting from area V2 to V4 in the macaque monkey. Cerebral Cortex 2, 353–374.

    PubMed  Google Scholar 

  • Rockland, K. S. (1995) Morphology of individual axons projecting from area V2 to MT in the macaque. Journal of Comparative Neurology 355, 15–26.

    PubMed  Google Scholar 

  • Rockland, K. S. (1997) Elements of cortical architecture: Hierarchy revisited. In Cerebral Cortex Vol. 12, Extrastriate Cortex in Primates (edited by Rockland, K., Kaas, J. H. &; Peters, A.) pp. 243–293. New York: Plenum.

    Google Scholar 

  • Rockland, K. S. &; Pandya, D. N. (1979) Laminar origins and terminations of cortical connections of the occipital lobe in the rhesus monkey. Brain Research 179, 3–20.

    PubMed  Google Scholar 

  • Rockland, K. S. &; Lund, J. S. (1982)Widespread periodic intrinsic connections in the tree shrew visual cortex. Science 215, 1532–1534.

    PubMed  Google Scholar 

  • Rockland, K. S. &; Lund, J. S. (1983) Intrinsic laminar lattice connections in primate visual cortex. Journal of Comparative Neurology 216, 303–318.

    PubMed  Google Scholar 

  • Rockland, K. S. &; Virga, A. (1990) Organization of individual cortical axons projecting from area V1 (area 17) to V2 (area 18) in the macaque monkey.Visual Neurscience 4, 11–28.

    Google Scholar 

  • Rockland, K. S., Lund, J. S. &; Humphrey, A. L. (1982) Anatomical banding of intrinsic connections in striate cortex of tree shrews (Tupaia glis). Journal of Comparative Neurology 209, 41–58.

    PubMed  Google Scholar 

  • Roe, A. &; Ts'o, D. Y. (1997) The functional architecture of area V2 in the macaque monkey: Physiology, topography and connectivity. In Cerebral Cortex Vol. 12, Extrastriate Cortex in Primates (edited by Rockland, K., Kaas, J. H. &; Peters, A.) pp. 295–333. New York: Plenum.

    Google Scholar 

  • Rosa, M. G. P. (1997) Visuotopic organization of primate extrastriate cortex. In Cerebral Cortex Vol. 12, Extrastriate Cortex in Primates (edited by Rockland, K., Kaas, J. H. &; Peters, A.) pp. 127–204. New York: Plenum.

    Google Scholar 

  • Sagase, Y., Yamane, S., Ueno, S. &; Kawano, K. (1999) Global and fine information coded by single neurons in the temporal visual cortex. Nature 400, 869–873.

    PubMed  Google Scholar 

  • Saleem, K. S., Tanaka, K. &; Rockland, K. S. (1993) Specific and columnar projection from area TEO to area TE in the macaque inferotemporal cortex. Cerebral Cortex 3, 454–464.

    PubMed  Google Scholar 

  • Sawatari, A. &; Callaway, E. M. (1996) Convergence of magno-and parvocellular pathways in layer 4b of macaque primary visual cortex. Nature 380, 442–446.

    PubMed  Google Scholar 

  • Schiller, P. H. (1996) On the specificity of neurons in visual areas. Behavioural Brain Research, 76, 21–35.

    PubMed  Google Scholar 

  • Segev, I. &; Rall, W. (1998) Excitable dendrites and spines: Earlier theoretical insights elucidate recent direct observations. Trends in Neuroscience 21, 453–460.

    Google Scholar 

  • Seltzer, B. &; Pandya, D. N. (1978) Afferent cortical connections of the superior temporal sulcus and surrounding cortex in the rhesus monkey. Brain Research 149, 1–24.

    PubMed  Google Scholar 

  • Singer, W. &; Gray, C. M. (1995) Visual feature integration and the temporal correlation hypothesis. Annual Reviews in Neuroscience 18, 555–586.

    Google Scholar 

  • Shipp, S. &; Zeki, S. (1989a) The organization of connections between area V5 and V2 in macaque monkey visual cortex. European Journal of Neuroscience 1, 333–354.

    PubMed  Google Scholar 

  • Shipp, S. &; Zeki, S. (1989b) The organization of connections between areas V5 and V1 in macaque monkey visual cortex. European Journal of Neuroscience 1, 309–332.

    PubMed  Google Scholar 

  • Sobotka, S. &; Ringo, J. L. (1993) Investigation of long term recognition and association memory in unit responses from inferotemporal cortex. Experimental Brain Research 96, 28–38.

    Google Scholar 

  • Somogyi, P., Cowey, A., HalÁsz, N. &; Freund, T. F. (1981) Vertical organization of neurones accumulating 3H-GABA in visual cortex of rhesus monkey. Nature 294, 761–763.

    PubMed  Google Scholar 

  • Somogyi, P., Tamas, G., Lujan, R. &; Buhl, E. H. (1998) Salient features of synaptic organisation in the cerebral cortex. Brain Research Reviews 26, 113–135.

    PubMed  Google Scholar 

  • Somogyi, P., Cowey, A., KisvÁrday, Z. F., Freund, T. F. &; SzentÁgothai, J. (1983) Retrograde transport of γ-amino[3H]butyric acid reveals specific interlaminar connections in the striate cortex of monkey. Proceedings of the National Academy of Science USA 80, 2385–2389.

    Google Scholar 

  • Stepanyants, A., Hof, P. R. &; Chklovskii, D. B. (2002) Geometry and structural plasticity of synaptic connectivity. Neuron 34, 275–288.

    PubMed  Google Scholar 

  • SzentÁgothai, J. (1975) The “module-concept” in cerebral cortex architecture. Brain Research 95, 475–496.

    PubMed  Google Scholar 

  • Tanaka, K., Koyama, T. &; Mikami, A. (1999) Neurons in the temporal cortex change their preferred direction of motion dependant on shape. NeuroReport 10, 393–397.

    PubMed  Google Scholar 

  • Taylor, W. R. &; Vaney, D. I. (2002) Diverse synaptic mechanisms generate direction selectivity in the rabbit retina. Journal of Neuroscience 22, 7712–7720.

    PubMed  Google Scholar 

  • Taylor, W. R., He, S., Levick, W. R., Vaney, D. I. (2000) Dendritic computation of direction selectivity by retinal ganglion cells. Science 289, 2347–2350.

    PubMed  Google Scholar 

  • Ts'o, D. Y. &; Gilbert, C. D. (1988) The organization of chromatic and spatial interactions in the primate striate cortex. Journal of Neuroscience 8, 1712–1727.

    PubMed  Google Scholar 

  • Ts'o, D. Y., Gilbert, C. D. &; Wiesel, T. N. (1986) Relationships between horizontal interactions and functional architecture in the cat striate cortex as revealed by cross-correlation analysis. Journal of Neuroscience 6, 1160–1170.

    PubMed  Google Scholar 

  • Ungerleider, L. G. &; Mishkin, M. (1982) Two cortical systems. In Analysis of Visual Behavior (edited by Ingle, D. J., Goodale, M. A. &; Mansfield, R. J.W.) pp. 549–586. Cambridge, MA: MIT Press.

    Google Scholar 

  • van Essen, D. C., Newsome, W. T., Maunsell, J. H. R. &; Bixby, J. L. (1986) The projections from striate cortex (V1) to areas V2 and V3 in the macaque monkey: Asymmetries, areal bounderies, and patchy connections. Journal of Comparative Neurology 244, 451–480.

    PubMed  Google Scholar 

  • Vaney, D. I. &; Taylor, W. R. (2002) Direction selectivity in the retina. Current Opinion in Neurobiology 12, 405–410.

    PubMed  Google Scholar 

  • Vogt Weisenhorn, D. M., Illing, R.-B. &; Spatz, W. B. (1995) Morphology and connections of neurons in area 17 projecting to the extrastriate areas MT and 19DM and to the superior colliculus in the monkey Callithrix jacchus. Journal of Comparative Neurology 362, 233–255.

    PubMed  Google Scholar 

  • von Economo, C. (1929) The Cytoarchitectonics of the Human Cerebral Cortex. Oxford: Humphrey Milford.

    Google Scholar 

  • Walker, A. E. (1940) A cytoarchitectural study of the prefrontal areas of the macaque monkey. Journal of Comparative Neurology 73, 59–86.

    Google Scholar 

  • Wang, Y., Fujita, I. &; Murayama, Y. (2000) Neuronal mechanisms of selectivity for object features revealed by blocking inhibition in inferotemporal cortex. Nature Neuroscience 3, 807–813.

    PubMed  Google Scholar 

  • Wang, Y., Fujita, I., Tamura, H. &; Murayama, Y. (2002) Contribution of GABAergic inhibition to receptive field structures of monkey inferior temporal neurons. Cerebral Cortex 12, 62–74.

    PubMed  Google Scholar 

  • Weller, R. E. (1988) Two cortical visual systems in Old World and New World primates. In Progress in Brain Research (edited by Hicks, T. P. &; Benedek, G.) pp. 293–306. Amsterdam: Elsevier.

    Google Scholar 

  • Yin, T. C. &; Mountcastle, V. B. (1977) Visual input to the visuomotor mechanisms of the monkey's parietal lobe. Science 197, 1381–1383.

    PubMed  Google Scholar 

  • Zilles, K. &; Clarke, S. (1997) Architecture, connectivity, and transmitter receptors of human extrastriate visual cortex. In Cerebral Cortex Vol. 12, Extrastriate Cortex in Primates (edited by Rockland, K., Kaas, J. H. &; Peters, A.) pp. 673–742. New York: Plenum.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Elston, G.N. Cortical heterogeneity: Implications for visual processing and polysensory integration. J Neurocytol 31, 317–335 (2002). https://doi.org/10.1023/A:1024182228103

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1024182228103

Keywords

Navigation