The primate connectome in context: Principles of connections of the cortical visual system

NeuroImage

Volumn 134, Issue , 2016, Pages 685-702

  Hilgetag, Claus C ^a,b   Medalla, Maria ^b,c   Beul, Sarah F ^a   Barbas, Helen ^b,c  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b BOSTON UNIVERSITY   (United States)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN CORTEX; CELL DENSITY; CONNECTOME; CORTICAL THICKNESS (BRAIN); FEEDBACK SYSTEM; MACACA; NERVE CELL; NERVE CELL NETWORK; NERVE PROJECTION; NEUROANATOMY; NONHUMAN; PREFRONTAL CORTEX; PRIMATE; PRIORITY JOURNAL; SENSORY NERVE; STATISTICAL ANALYSIS; STRUCTURAL HOMOLOGY; VISUAL CORTEX; VISUAL SYSTEM; ANATOMY AND HISTOLOGY; ANIMAL; BIOLOGICAL MODEL; CELL COUNT; CYTOLOGY; NERVE TRACT;

ANIMALS; CELL COUNT; CONNECTOME; MACACA; MODELS, NEUROLOGICAL; NEURAL PATHWAYS; NEURONS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84975487216     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2016.04.017     Document Type: Article

References (106)

1. Ainsworth, M., Lee, S., Cunningham, M.O., Traub, R.D., Kopell, N.J., Whittington, M.A., Rates and rhythms: a synergistic view of frequency and temporal coding in neuronal networks. Neuron 75 (2012), 572–583.
2. Anderson, M.C., Bunce, J.G., Barbas, H., Prefrontal-hippocampal pathways underlying inhibitory control over memory. Neurobiol. Learn. Mem., 2015 (Nov 28. pii: S1074-7427(15) 00217-8).
3. Barbas, H., Pattern in the laminar origin of corticocortical connections. J. Comp. Neurol. 252 (1986), 415–422.
4. Barbas, H., Anatomic organization of basoventral and mediodorsal visual recipient prefrontal regions in the rhesus monkey. J. Comp. Neurol. 276 (1988), 313–342.
5. Barbas, H., Organization of cortical afferent input to orbitofrontal areas in the rhesus monkey. Neuroscience 56 (1993), 841–864.
6. Barbas, H., Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci. Biobehav. Rev. 19 (1995), 499–510.
7. Barbas, H., Connections underlying the synthesis of cognition, memory, and emotion in primate prefrontal cortices. Brain Res. Bull. 52 (2000), 319–330.
8. Barbas, H., General cortical and special prefrontal connections: principles from structure to function. Annu. Rev. Neurosci. 38 (2015), 269–289.
9. Barbas, H., García-Cabezas, M.A., Motor cortex layer 4: less is more. Trends Neurosci. 38 (2015), 259–261.
10. Barbas, H., Mesulam, M.M., Organization of afferent input to subdivisions of area 8 in the Rhesus monkey. J. Comp. Neurol. 200 (1981), 407–431.
11. Barbas, H., Pandya, D., Architecture and intrinsic connections of the prefrontal cortex in the Rhesus monkey. J. Comp. Neurol. 286 (1989), 353–375.
12. Barbas, H., Rempel-Clower, N., Cortical structure predicts the pattern of corticocortical connections. Cereb. Cortex 7 (1997), 635–646.
13. Barbas, H., Ghashghaei, H., Dombrowski, S.M., Rempel-Clower, N.L., Medial prefrontal cortices are unified by common connections with superior temporal cortices and distinguished by input from memory-related areas in the rhesus monkey. J. Comp. Neurol. 410 (1999), 343–367.
14. Barbas, H., Hilgetag, C.C., Saha, S., Dermon, C.R., Suski, J.L., Parallel organization of contralateral and ipsilateral prefrontal cortical projections in the rhesus monkey. BMC Neurosci., 6, 2005, 32.
15. Barbas, H., Medalla, M., Alade, O., Suski, J., Zikopoulos, B., Lera, P., Relationship of prefrontal connections to inhibitory systems in superior temporal areas in the rhesus monkey. Cereb. Cortex 15 (2005), 1356–1370.
16. Barone, P., Batardiere, A., Knoblauch, K., Kennedy, H., Laminar distribution of neurons in extrastriate areas projecting to visual areas V1 and V4 correlates with the hierarchical rank and indicates the operation of a distance rule. J. Neurosci. 20 (2000), 3263–3281.
17. Bassett, D.S., Bullmore, E.T., Human brain networks in health and disease. Curr. Opin. Neurol. 22 (2009), 340–347.
18. Bassett, D.S., Bullmore, E., Verchinski, B.A., Mattay, V.S., Weinberger, D.R., Meyer-Lindenberg, A., Hierarchical organization of human cortical networks in health and schizophrenia. J. Neurosci. 28 (2008), 9239–9248.
19. Bastos, A.M., Vezoli, J., Bosman, C.A., Schoffelen, J.M., Oostenveld, R., Dowdall, J.R., De Weerd, P., Kennedy, H., Fries, P., Visual areas exert feedforward and feedback influences through distinct frequency channels. Neuron 85 (2015), 390–401.
20. Benes, F.M., Vincent, S.L., Todtenkopf, M., The density of pyramidal and nonpyramidal neurons in anterior cingulate cortex of schizophrenic and bipolar subjects. Biol. Psychiatry 50 (2001), 395–406.
21. Beul, S.F., Hilgetag, C.C., Towards a “canonical” agranular cortical microcircuit. Front. Neuroanat., 8, 2015, 165.
22. Beul, S.F., Grant, S., Hilgetag, C.C., A predictive model of the cat cortical connectome based on cytoarchitecture and distance. Brain Struct. Funct. 220 (2015), 3167–3184.
23. Boussaoud, D., Desimone, R., Ungerleider, L.G., Visual topography of area TEO in the macaque. J. Comp. Neurol. 306 (1991), 554–575.
24. Bullier, J., Nowak, L.G., Parallel versus serial processing: new vistas on the distributed organization of the visual system. Curr. Opin. Neurobiol. 5 (1995), 497–503.
25. Bullmore, E., Sporns, O., Complex brain networks: graph theoretical analysis of structural and functional systems. Nat. Rev. Neurosci. 10 (2009), 186–198.
26. Bunce, J.G., Barbas, H., Prefrontal pathways target excitatory and inhibitory systems in memory-related medial temporal cortices. NeuroImage 55 (2011), 1461–1474.
27. Bunce, J.G., Zikopoulos, B., Feinberg, M., Barbas, H., Parallel prefrontal pathways reach distinct excitatory and inhibitory systems in memory-related rhinal cortices. J. Comp. Neurol. 521 (2013), 4260–4283.
28. Chen, Y., Wang, S., Hilgetag, C.C., Zhou, C., Trade-off between multiple constraints enables simultaneous formation of modules and hubs in neural systems. PLoS Comput. Biol., 9(3), 2013, e1002937.
29. Collins, C.E., Airey, D.C., Young, N.A., Leitch, D.B., Kaas, J.H., Neuron densities vary across and within cortical areas in primates. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 15927–15932.
30. Ding, S.-L., Van Hoesen, G.W., Borders, extent, and topography of human perirhinal cortex as revealed using multiple modern neuroanatomical and pathological markers. Hum. Brain Mapp. 31 (2010), 1359–1379.
31. Dombrowski, S.M., Hilgetag, C.C., Barbas, H., Quantitative architecture distinguishes prefrontal cortical systems in the rhesus monkey. Cereb. Cortex 11 (2001), 975–988.
32. Donoghue, M.J., Rakic, P., Molecular gradients and compartments in the embryonic primate cerebral cortex. Cereb. Cortex 9 (1999), 586–600.
33. Ercsey-Ravasz, M., Markov, N.T., Lamy, C., Van Essen, D.C., Knoblauch, K., Toroczkai, Z., Kennedy, H., A predictive network model of cerebral cortical connectivity based on a distance rule. Neuron 80 (2013), 184–197.
34. Felleman, D.J., Van Essen, D.C., Distributed hierarchical processing in the primate cerebral cortex. Cereb. Cortex 1 (1991), 1–47.
35. Floyd, R.W., Algorithm 97: shortest path. Commun. ACM, 5, 1962, 345.
36. Friston, K., A theory of cortical responses. Philos. Trans. R. Soc. B 360 (2005), 815–836.
37. García-Cabezas, M.Á., Barbas, H., Area 4 has layer IV in adult primates. Eur. J. Neurosci. 39 (2014), 1824–1834.
38. Grant, S., Hilgetag, C.C., Graded classes of cortical connections: quantitative analyses of laminar projections to motion areas of cat extrastriate cortex. Eur. J. Neurosci. 22 (2005), 681–696.
39. Gundersen, H.J., Bagger, P., Bendtsen, T.F., Evans, S.M., Korbo, L., Marcussen, N., Møller, A., Nielsen, K., Nyengaard, J.R., Pakkenberg, B., Sørensen, F.B., Vesterby, A., West, M.J., The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96 (1988), 857–881.
40. He, Y., Chen, Z.J., Evans, A.C., Small-world anatomical networks in the human brain revealed by cortical thickness from MRI. Cereb. Cortex 17 (2007), 2407–2419.
41. He, Y., Chen, Z., Evans, A., Structural insights into aberrant topological patterns of large-scale cortical networks in Alzheimer's disease. J. Neurosci. 28 (2008), 4756–4766.
42. He, Y., Dagher, A., Chen, Z., Charil, A., Zijdenbos, A., Worsley, K., Evans, A., Impaired small-world efficiency in structural cortical networks in multiple sclerosis associated with white matter lesion load. Brain 132 (2009), 3366–3379.
43. Hegdé, J., Felleman, D.J., Reappraising the functional implications of the primate visual anatomical hierarchy. Neuroscientist 13 (2007), 416–421.
44. Hilgetag, C.C., Barbas, H., Developmental mechanics of the primate cerebral cortex. Anat. Embryol. 210 (2005), 411–417.
45. Hilgetag, C.C., Barbas, H., Role of mechanical factors in the morphology of the primate cerebral cortex. PLoS Comput. Biol., 2, 2006, e22.
46. Hilgetag, C.C., Grant, S., Uniformity, specificity and variability of corticocortical connectivity. Philos. Trans. R. Soc. B 355 (2000), 7–20.
47. Hilgetag, C.C., Grant, S., Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51 (2010), 1006–1017.
48. Hilgetag, C.C., O'Neill, M.A., Young, M.P., Indeterminate organization of the visual system. Science 271 (1996), 776–777.
49. Hilgetag, C.C., Burns, G.A.P.C., O'Neill, M.A., Scannell, J.W., Young, M.P., Anatomical connectivity defines the organization of clusters of cortical areas in the macaque and the cat. Philos. Trans. R. Soc. B 355 (2000), 91–110.
50. Hilgetag, C.C., O'Neill, M.A., Young, M.P., Hierarchical organization of macaque and cat cortical sensory systems explored with a novel network processor. Philos. Trans. R. Soc. B 355 (2000), 71–89.
51. Hilgetag, C.C., Dombrowski, S.M., Barbas, H., Classes and gradients of prefrontal cortical organization in the primate. Neurocomputing 44-46 (2002), 823–829.
52. Hilgetag, C.C., Medalla, M., Barbas, H., Relationship of connection patterns to the architecture of the primate visual cortex. Soc. Neurosci. Abstr., 34, 2008, 215.2.
53. Howard, C.V., Reed, M.G., Unbiased Stereology, Three-dimensional Measurement in Microscopy. 1998, BIOS Scientific Publishers Limited, Oxford.
54. Hyvarinen, J., Regional distribution of functions in parietal association area 7 of the monkey. Brain Res. 206 (1981), 287–303.
55. Kaiser, M., Hilgetag, C.C., Nonoptimal component placement, but short processing paths, due to long-distance projections in neural systems. PLoS Comput. Biol., 2, 2006, e95.
56. Kaiser, M., Hilgetag, C.C., Development of multi-cluster cortical networks by time windows for spatial growth. Neurocomputing 70 (2007), 1829–1832.
57. Kaiser, M., Hilgetag, C.C., van Ooyen, A., A simple rule for axon outgrowth and synaptic competition generates realistic connection lengths and filling fractions. Cereb. Cortex 19 (2009), 3001–3010.
58. Klyachko, V.A., Stevens, C.F., Connectivity optimization and the positioning of cortical areas. Proc. Natl. Acad. Sci. U. S. A. 100 (2003), 7937–7941.
59. Lakatos, P., Karmos, G., Mehta, A.D., Ulbert, I., Schroeder, C.E., Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320 (2008), 110–113.
60. Lerch, J.P., Worsley, K., Shaw, W.P., Greenstein, D.K., Lenroot, R.K., Giedd, J., Evans, A.C., Mapping anatomical correlations across cerebral cortex (MACACC) using cortical thickness from MRI. NeuroImage 31 (2006), 993–1003.
61. Lim, S., Kaiser, M., Developmental time windows for axon growth influence neuronal network topology. Biol. Cybern. 109 (2015), 275–286.
62. Liu, Y., Liang, M., Zhou, Y., He, Y., Hao, Y., Song, M., Yu, C., Liu, H., Liu, Z., Jiang, T., Disrupted small-world networks in schizophrenia. Brain 131 (2008), 945–961.
63. Lukaszewicz, A., Cortay, V., Giroud, P., Berland, M., Smart, I., Kennedy, H., Dehay, C., The concerted modulation of proliferation and migration contributes to the specification of the cytoarchitecture and dimensions of cortical areas. Cereb. Cortex 16:Suppl. 1 (2006), i26–i34.
64. MacNeil, M.A., Lomber, S.G., Payne, B.R., Thalamic and cortical projections to middle suprasylvian cortex of cats: constancy and variation. Exp. Brain Res. 114 (1997), 24–32.
65. Marín-Padilla, M., Early prenatal ontogenesis of the cerebral cortex (neocortex) of the cat (Felis domestica). A Golgi study. I. The primordial neocortical organization. Z. Anat. Entwicklungsgesch. 134 (1971), 117–145.
66. Markov, N.T., Misery, P., Falchier, A., Lamy, C., Vezoli, J., Quilodran, R., Gariel, M.A., Giroud, P., Ercsey-Ravasz, M., Pilaz, L.J., Huissoud, C., Barone, P., Dehay, C., Toroczkai, Z., Van Essen, D.C., Kennedy, H., Knoblauch, K., Weight consistency specifies regularities of macaque cortical networks. Cereb. Cortex 21 (2011), 1254–1272.
67. Markov, N.T., Ercsey-Ravasz, M., Lamy, C., Ribeiro Gomes, A.R., Magrou, L., Misery, P., Giroud, P., Barone, P., Dehay, C., Toroczkai, Z., Knoblauch, K., Van Essen, D.C., Kennedy, H., The role of long-range connections on the specificity of the macaque interareal cortical network. Proc. Natl. Acad. Sci. 110 (2013), 5187–5192.
68. Markov, N.T., Vezoli, J., Chameau, P., Falchier, A., Quilodran, R., Huissoud, C., Lamy, C., Misery, P., Giroud, P., Ullman, S., Barone, P., Dehay, C., Knoblauch, K., Kennedy, H., Anatomy of hierarchy: feedforward and feedback pathways in macaque visual cortex. J. Comp. Neurol. 522 (2014), 225–259.
69. Medalla, M., Barbas, H., Diversity of laminar connections linking periarcuate and lateral intraparietal areas depends on cortical structure. Eur. J. Neurosci. 23 (2006), 161–179.
70. Medalla, M., Barbas, H., Synapses with inhibitory neurons differentiate anterior cingulate from dorsolateral prefrontal pathways associated with cognitive control. Neuron 61 (2009), 609–620.
71. Medalla, M., Barbas, H., Anterior cingulate synapses in prefrontal areas 10 and 46 suggest differential influence in cognitive control. J. Neurosci. 30 (2010), 16068–16081.
72. Mesulam, M.M., From sensation to cognition. Brain 121:Pt 6 (1998), 1013–1052.
73. Mesulam, M., Representation, inference, and transcendent encoding in neurocognitive networks of the human brain. Ann. Neurol. 64 (2008), 367–378.
74. Michalareas, G., Vezoli, J., van Pelt, S., Schoffelen, J.M., Kennedy, H., Fries, P., Alpha-beta and gamma rhythms subserve feedback and feedforward influences among human visual cortical areas. Neuron 89 (2016), 384–397.
75. Neal, J.W., Pearson, R.C., Powell, T.P., The cortico-cortical connections within the parieto-temporal lobe of area PG, 7a, in the monkey. Brain Res. 438 (1988), 343–350.
76. O'Kusky, J., Colonnier, M., A laminar analysis of the number of neurons, glia, and synapses in the visual cortex (area 17) of adult macaque monkeys. J. Comp. Neurol. 210 (1982), 278–290.
77. Pandya, D.N., Seltzer, B., Barbas, H., Input-output organization of the primate cerebral cortex. Steklis, H.D., Erwin, J., (eds.) Comparative Primate Biology, Neurosciences., Vol. 4, 1988, Alan R. Liss, New York, 39–80.
78. Petroni, F., Panzeri, S., Hilgetag, C.C., Kötter, R., Young, M.P., Simultaneity of responses in a hierarchical visual network. Neuroreport 12 (2001), 2753–2759.
79. Raichle, M., The restless brain. Brain Connect. 1 (2011), 3–12.
80. Rakic, P., Neurogenesis in adult primate neocortex: an evaluation of the evidence. Nat. Rev. Neurosci. 3 (2002), 65–71.
81. Reid, A.T., Krumnack, A., Wanke, E., Kötter, R., Optimization of cortical hierarchies with continuous scales and ranges. NeuroImage 47 (2009), 611–617.
82. Rempel-Clower, N.L., Barbas, H., The laminar pattern of connections between prefrontal and anterior temporal cortices in the Rhesus monkey is related to cortical structure and function. Cereb. Cortex 10 (2000), 851–865.
83. Saleem, K.S., Price, J.L., Hashikawa, T., Cytoarchitectonic and chemoarchitectonic subdivisions of the perirhinal and parahippocampal cortices in macaque monkeys. J. Comp. Neurol. 500 (2007), 973–1006.
84. Scannell, J.W., Grant, S., Payne, B.R., Baddeley, R., On variability in the density of corticocortical and thalamocortical connections. Philos. Trans. R. Soc. B 355 (2000), 21–35.
85. Schall, J.D., Morel, A., King, D.J., Bullier, J., Topography of visualcortex connections with frontal eye field in macaque: convergence and segregation of processing streams. J. Neurosci. 15 (1995), 4464–4487.
86. Schmitz, C., Hof, P.R., Design-based stereology in neuroscience. Neuroscience 130 (2005), 813–831.
87. Schmolesky, M.T., Wang, Y., Hanes, D.P., Thompson, K.G., Leutgeb, S., Schall, J.D., Leventhal, A.G., Signal timing across the macaque visual system. J. Neurophysiol. 79 (1998), 3272–3278.
88. Scholtens, L.H., Schmidt, R., de Reus, M.A., van den Heuvel, M.P., Linking macroscale graph analytical organization to microscale neuroarchitectonics in the macaque connectome. J. Neurosci. 34 (2014), 12192–12205.
89. Seltzer, B., Pandya, D.N., Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey. Brain Res. 192 (1980), 339–351.
90. Sporns, O., Networks of the Brain. 2010, MIT Press.
91. Sporns, O., Chialvo, D.R., Kaiser, M., Hilgetag, C.C., Organization, development and function of complex brain networks. Trends Cogn. Sci. 8 (2004), 418–425.
92. Stanton, G.B., Bruce, C.J., Goldberg, M.E., Topography of projections to posterior cortical areas from the macaque frontal eye fields. J. Comp. Neurol. 353 (1995), 291–305.
93. Suzuki, W.A., Amaral, D.G., Perirhinal and parahippocampal cortices of the macaque monkey: cytoarchitectonic and chemoarchitectonic organization. J. Comp. Neurol. 463 (2003), 67–91.
94. Takahata, T., Komatsu, Y., Watakabe, A., Hashikawa, T., Tochitani, S., Yamamori, T., Differential expression patterns of occ1-related genes in adult monkey visual cortex. Cereb. Cortex 19 (2009), 1937–1951.
95. Ungerleider, L.G., Galkin, T.W., Desimone, R., Gattass, R., Cortical connections of area V4 in the macaque. Cereb. Cortex 18 (2008), 477–499.
96. Van Essen, D.C., Smith, S.M., Barch, D.M., Behrens, T.E.J., Yacoub, E., Ugurbil, K., for the WU-Minn HCP Consortium, The WU-Minn human connectome project: an overview. NeuroImage 80 (2013), 62–79.
97. Van Hoesen, G.W., Pandya, D.N., Some connections of the entorhinal (area 28) and perirhinal (area 35) cortices of the rhesus monkey. III. Efferent connections. Brain Res. 95 (1975), 39–59.
98. Vanduffel, W., Payne, B.R., Lomber, S.G., Orban, G.A., Functional impact of cerebral connections. Proc. Natl. Acad. Sci. U. S. A. 94 (1997), 7617–7620.
99. Varier, S., Kaiser, M., Neural development features: spatio-temporal development of the Caenorhabditis elegans neuronal network. PLoS Comput. Biol., 7, 2011, e1001044.
100. Von Economo, C.F., Zellaufbau der Grosshirnrinde des Menschen. 1927, Springer, Berlin.
101. Wang, X.J., Tegnér, J., Constantinidis, C., Goldman-Rakic, P.S., Division of labor among distinct subtypes of inhibitory neurons in a cortical microcircuit of working memory. Proc. Natl. Acad. Sci. U. S. A. 101:5 (2004), 1368–1373.
102. Worsley, K.J., Chen, J.-I., Lerch, J., Evans, A.C., Comparing functional connectivity via thresholding correlations and singular value decomposition. Philos. Trans. R. Soc. B 360 (2005), 913–920.
103. Young, M., Objective analysis of the topological organization of the primate cortical visual system. Nature 358 (1992), 152–155.
104. Zikopoulos, B., Barbas, H., Changes in prefrontal axons may disrupt the network in autism. J. Neurosci. 30 (2010), 14595–14609.
105. Zikopoulos, B., Barbas, H., Altered neural connectivity in excitatory and inhibitory cortical circuits in autism. Front. Hum. Neurosci., 7, 2013, 609.
106. Zilles, K., Amunts, K., Segregation and wiring in the brain. Science 335 (2012), 1582–1584.