Multimodal analysis of cortical chemoarchitecture and macroscale fMRI resting-state functional connectivity

Human Brain Mapping

Volumn 37, Issue 9, 2016, Pages 3103-3113

  van den Heuvel, Martijn P ^a   Scholtens, Lianne H ^a   Turk, Elise ^a   Mantini, Dante ^b,c,d   Vanduffel, Wim ^b,e   Feldman Barrett, Lisa ^f,g  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b KU LEUVEN UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d ETH ZURICH   (Switzerland)

^e HARVARD MEDICAL SCHOOL   (United States)

^f NORTHEASTERN UNIVERSITY   (United States)

^g MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

chemoarchitecture; connectome; excitatory; fMRI; functional connectivity; inhibitory; receptor; resting state fMRI

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; AMPA RECEPTOR; MUSCARINIC M1 RECEPTOR; MUSCARINIC M2 RECEPTOR;

ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN CORTEX; BRAIN REGION; CONNECTOME; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; HUMAN TISSUE; MACACA; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DENSITY; RESTING STATE NETWORK;

EID: 84982994337     PISSN: 10659471     EISSN: 10970193     Source Type: Journal    
DOI: 10.1002/hbm.23229     Document Type: Article

References (81)

1. Adachi Y, Osada T, Sporns O, Watanabe T, Matsui T, Miyamoto K, Miyashita Y (2012): Functional connectivity between anatomically unconnected areas is shaped by collective network-level effects in the macaque cortex. Cereb Cortex 22:1586–1592.
2. Amunts K, Lenzen M, Friederici AD, Schleicher A, Morosan P, Palomero-Gallagher N, Zilles K (2010): Broca's region: Novel organizational principles and multiple receptor mapping. PLoS Biol 8:e1000489.
3. Arrubla J, Tse DH, Amkreutz C, Neuner I, Shah NJ (2014): GABA concentration in posterior cingulate cortex predicts putamen response during resting state fMRI. PLoS One 9:e106609.
4. Baggio HC, Segura B, Junque C, de Reus MA, Sala-Llonch R, Van den Heuvel MP (2015): Rich club organization and cognitive performance in healthy older participants. J Cogn Neurosci 27:1801–1810.
5. Barbas H, Rempel-Clower N (1997): Cortical structure predicts the pattern of corticocortical connections. Cereb Cortex 7:635–646.
6. Barenne J. (1924): Experimental Researches on Sensory Localization in the Cerebral Cortex of the Monkey (Macacus). Proceedings of the Royal Society B: Biological Sciences 96:272–291.
7. Bassett DS, Bullmore ET, Meyer-Lindenberg A, Apud JA, Weinberger DR, Coppola R (2009): Cognitive fitness of cost-efficient brain functional networks. Proc Natl Acad Sci USA 106:11747–11752.
8. Beul SF, Grant S, Hilgetag CC (2015): A predictive model of the cat cortical connectome based on cytoarchitecture and distance. Brain Struct Funct 220:3167–3184.
9. Biswal B, Yetkin FZ, Haughton VM, Hyde JS (1995): Functional connectivity in the motor cortex of resting human brain using echo-planar MRI. Magn Reson Med 34:537–541.
10. Bohlken MM, Mandl RC, Brouwer RM, van den Heuvel MP, Hedman AM, Kahn RS, Hulshoff Pol HE (2014): Heritability of structural brain network topology: A DTI study of 156 twins. Hum Brain Mapp 35:5295–5305.
11. Cammoun L, Gigandet X, Meskaldji D, Thiran JP, Sporns O, Do KQ, Maeder P, Meuli R, Hagmann P (2011): Mapping the human connectome at multiple scales with diffusion spectrum MRI. J Neurosci Methods 203:386–397.
12. Caspers J, Palomero-Gallagher N, Caspers S, Schleicher A, Amunts K, Zilles K (2015): Receptor architecture of visual areas in the face and word-form recognition region of the posterior fusiform gyrus. Brain Struct Funct 220:205–219.
13. Caspers S, Schleicher A, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Zilles K (2013): Organization of the human inferior parietal lobule based on receptor architectonics. Cereb Cortex 23:615–628.
14. Cioli C, Abdi H, Beaton D, Burnod Y, Mesmoudi S (2014): Differences in human cortical gene expression match the temporal properties of large-scale functional networks. PLoS One 9:e115913.
15. Cocchi L, Harding IH, Lord A, Pantelis C, Yucel M, Zalesky A (2014): Disruption of structure-function coupling in the schizophrenia connectome. NeuroImage Clin 4:779–787.
16. Cole MW, Yarkoni T, Repovs G, Anticevic A, Braver TS (2012): Global connectivity of prefrontal cortex predicts cognitive control and intelligence. J Neurosci 32:8988–8999.
17. Collin G, Kahn RS, de Reus MA, Cahn W, van den Heuvel MP (2014): Impaired rich club connectivity in unaffected siblings of schizophrenia patients. Schizophr Bull 40:438–448.
18. Collin G, de Nijs J, Hulshoff Pol HE, Cahn W, van den Heuvel MP. (2015): Connectome organization is related to longitudinal changes in general functioning, symptoms and IQ in chronic schizophrenia. Schizophrenia Research (Epub ahead of print).
19. Conner CR, Ellmore TM, Pieters TA, DiSano MA, Tandon N (2011): Variability of the relationship between electrophysiology and BOLD-fMRI across cortical regions in humans. J Neurosci 31:12855–12865.
20. Contractor A, Mulle C, Swanson GT (2011): Kainate receptors coming of age: Milestones of two decades of research. Trends Neurosci 34:154–163.
21. Davis FC, Knodt AR, Sporns O, Lahey BB, Zald DH, Brigidi BD, Hariri AR (2013): Impulsivity and the modular organization of resting-state neural networks. Cereb Cortex 23:1444–1452.
22. De Barenne JD, McCulloch WS (1938): Functional organization in the sensory cortex of the monkey (Macaca mulatta). J Neurophysiol 1:16.
23. de Reus MA, van den Heuvel MP (2014): Simulated rich club lesioning in brain networks: A scaffold for communication and integration? Front Hum Neurosci 8:647.
24. Desikan RS, Segonne F, Fischl B, Quinn BT, Dickerson BC, Blacker D, Buckner RL, Dale AM, Maguire RP, Hyman BT, Albert MS, Killiany RJ (2006): An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980.
25. Duncan NW, Enzi B, Wiebking C, Northoff G (2011): Involvement of glutamate in rest-stimulus interaction between perigenual and supragenual anterior cingulate cortex: A combined fMRI-MRS study. Hum Brain Mapp 32:2172–2182.
26. Duncan NW, Wiebking C, Tiret B, Marjanska M, Hayes DJ, Lyttleton O, Doyon J, Northoff G (2013): Glutamate concentration in the medial prefrontal cortex predicts resting-state cortical-subcortical functional connectivity in humans. PLoS One 8:e60312.
27. Enzi B, Duncan NW, Kaufmann J, Tempelmann C, Wiebking C, Northoff G (2012): Glutamate modulates resting state activity in the perigenual anterior cingulate cortex—A combined fMRI-MRS study. Neuroscience 227:102–109.
28. Esslinger C, Walter H, Kirsch P, Erk S, Schnell K, Arnold C, Haddad L, Mier D, Opitz von Boberfeld C, Raab K, Witt SH, Rietschel M, Cichon S, Meyer-Lindenberg A (2009): Neural mechanisms of a genome-wide supported psychosis variant. Science 324:605.
29. Fischl B, Dale AM (2000): Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055.
30. Fornito A, Zalesky A, Bassett DS, Meunier D, Ellison-Wright I, Yucel M, Wood SJ, Shaw K, O'Connor J, Nertney D, Mowry BJ, Pantelis C, Bullmore ET (2011): Genetic influences on cost-efficient organization of human cortical functional networks. J Neurosci 31:3261–3270.
31. Fox MD, Raichle ME (2007): Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging. Nat Rev 8:700–711.
32. Friston KJ, Frith CD, Liddle PF, Frackowiak RS (1993): Functional connectivity: The principal-component analysis of large (PET) data sets. J Cereb Blood Flow Metab 13:5–14.
33. Glahn DC, Winkler AM, Kochunov P, Almasy L, Duggirala R, Carless MA, Curran JC, Olvera RL, Laird AR, Smith SM, Beckmann CF, Fox PT, Blangero J (2010): Genetic control over the resting brain. Proc Natl Acad Sci USA 107:1223–1228.
34. Hagmann P, Cammoun L, Gigandet X, Meuli R, Honey CJ, Wedeen VJ, Sporns O (2008): Mapping the structural core of human cerebral cortex. PLoS Biol 6:e159.
35. Hilgetag CC, Grant S (2010): Cytoarchitectural differences are a key determinant of laminar projection origins in the visual cortex. NeuroImage 51:1006–1017.
36. Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009): Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:2035–2040.
37. Horwitz B (2004): Relating fMRI and PET signals to neural activity by means of large-scale neural models. Neuroinformatics 2:251–266.
38. Jahanshad N, Rajagopalan P, Hua X, Hibar DP, Nir TM, Toga AW, Jack CR Jr, Saykin AJ, Green RC, Weiner MW, Medland SE, Montgomery GW, Hansell NK, McMahon KL, de Zubicaray GI, Martin NG, Wright MJ, Thompson PM, Alzheimer's Disease Neuroimaging I (2013): Genome-wide scan of healthy human connectome discovers SPON1 gene variant influencing dementia severity. Proc Natl Acad Sci USA 110:4768–4773.
39. Kandel ER, Schwartz JH, Jessell TM. (2000): Principles of neural science: McGraw-hill New York.
40. Kapogiannis D, Reiter DA, Willette AA, Mattson MP (2013): Posteromedial cortex glutamate and GABA predict intrinsic functional connectivity of the default mode network. NeuroImage 64:112–119.
41. Kong, F., Liu, L., Wang, X., Hu, S., Song, Y., Liu, J. (2015) Different neural pathways linking personality traits and eudaimonic well-being: A resting-state functional magnetic resonance imaging study. Cogn Affect Behav Neurosci 15:299–309.
42. Kötter R, Stephan KE, Palomero-Gallagher N, Geyer S, Schleicher A, Zilles K (2001): Multimodal characterisation of cortical areas by multivariate analyses of receptor binding and connectivity data. Anatomy Embryol 204:333–350.
43. Kötter R, Maier J, Margas W, Zilles K, Schleicher A, Bozkurt A (2007): Databasing receptor distributions in the brain. Methods Mol Biol 401:267–284.
44. Kunisato Y, Okamoto Y, Okada G, Aoyama S, Nishiyama Y, Onoda K, Yamawaki S (2011): Personality traits and the amplitude of spontaneous low-frequency oscillations during resting state. Neurosci Lett 492:109–113.
45. Logothetis NK (2002): The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philo Trans R Soc London 357:1003–1037.
46. Logothetis NK, Wandell BA (2004): Interpreting the BOLD signal. Annu Rev Physiol 66:735–769.
47. Logothetis NK, Pauls J, Augath M, Trinath T, Oeltermann A (2001): Neurophysiological investigation of the basis of the fMRI signal. Nature 412:150–157.
48. Lynall ME, Bassett DS, Kerwin R, McKenna PJ, Kitzbichler M, Muller U, Bullmore E (2010): Functional connectivity and brain networks in schizophrenia. J Neurosci 30:9477–9487.
49. Mantini D, Gerits A, Nelissen K, Durand JB, Joly O, Simone L, Sawamura H, Wardak C, Orban GA, Buckner RL, Vanduffel W (2011): Default mode of brain function in monkeys. J Neurosci 31:12954–12962.
50. Mantini D, Corbetta M, Romani GL, Orban GA, Vanduffel W (2013): Evolutionarily novel functional networks in the human brain? J Neurosci 33:3259–3275.
51. Miao X, Wu X, Li R, Chen K, Yao L (2011): Altered connectivity pattern of hubs in default-mode network with Alzheimer's disease: An Granger causality modeling approach. PLoS One 6:e25546.
52. Niessing J, Ebisch B, Schmidt KE, Niessing M, Singer W, Galuske RA (2005): Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309:948–951.
53. Park HJ, Friston K (2013): Structural and functional brain networks: From connections to cognition. Science 342:1238411.
54. Power JD, Barnes KA, Snyder AZ, Schlaggar BL, Petersen SE (2012): Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion. NeuroImage 59:2142–2154.
55. Rubinov M, Sporns O (2010): Complex network measures of brain connectivity: Uses and interpretations. NeuroImage 52:1059–1069.
56. Scheidegger M, Walter M, Lehmann M, Metzger C, Grimm S, Boeker H, Boesiger P, Henning A, Seifritz E (2012): Ketamine decreases resting state functional network connectivity in healthy subjects: Implications for antidepressant drug action. PLoS One 7:e44799.
57. Scholtens LH, de Reus M., van den Heuvel MP (2015): Linking contemporary high resolution magnetic resonance imaging to the von economo legacy: A study on the comparison of MRI cortical thickness and histological measurements of cortical structure. Hum Brain Mapp 36:3038–3046.
58. Scholtens LH, Schmidt R, de Reus MA, van den Heuvel MP (2014): Linking Macroscale Graph Analytical Organization to Microscale Neuroarchitectonics in the Macaque Connectome. J Neurosci 34:12192–12205.
59. Shmuel A, Leopold DA (2008): Neuronal correlates of spontaneous fluctuations in fMRI signals in monkey visual cortex: Implications for functional connectivity at rest. Hum Brain Mapp. 29:751–761.
60. Stagg CJ, Bachtiar V, Amadi U, Gudberg CA, Ilie AS, Sampaio-Baptista C, O'Shea J, Woolrich M, Smith SM, Filippini N, Near J, Johansen-Berg H (2014): Local GABA concentration is related to network-level resting functional connectivity. eLife 3:e01465.
61. Stephan KE, Friston KJ (2010): Analyzing effective connectivity with fMRI. Wiley Interdiscip Rev Cogn Sci 1:446–459.
62. Stephan KE, Hilgetag CC, Burns GA, O'Neill MA, Young MP, Kötter R (2000): Computational analysis of functional connectivity between areas of primate cerebral cortex. Philos Trans R Soc London 355:111–126.
63. Turk E, Scholtens LH, van den Heuvel MP (2016): Cortical chemoarchitecture shapes macroscale stimulating functional connectivity patterns in macaque cerebral cortex. Hum Brain Mapp 37:1856–1865.
64. van den Heuvel MP, Hulshoff Pol HE (2010a): Exploring the brain network: A review on resting-state fMRI functional connectivity. Eur Neuropsychopharmacol 20:519–534.
65. van den Heuvel MP, Hulshoff Pol HE (2010b): Specific somatotopic organization of functional connections of the primary motor network during resting state. Hum Brain Mapp 31:631–644.
66. van den Heuvel MP, Sporns O (2013a): An anatomical infrastructure for integration between functional networks in human cerebral cortex. J Neurosci 33:11.
67. van den Heuvel MP, Sporns O (2013b): Network hubs in the human brain. Trends Cogn Sci 17:683–696.
68. van den Heuvel MP, Stam CJ, Kahn RS, Hulshoff Pol HE (2009): Efficiency of functional brain networks and intellectual performance. J Neurosci 29:7619–7624.
69. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goni J, Hulshoff Pol HE, Kahn RS (2013a): Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70:783–792.
70. van den Heuvel MP, van Soelen IL, Stam CJ, Kahn RS, Boomsma DI, Hulshoff Pol HE (2013b): Genetic control of functional brain network efficiency in children. Eur Neuropsychopharmacol 23:19–23.
71. van den Heuvel MP, de Reus MA, Feldman Barrett L, Scholtens LH, Coopmans FMT, SChmidt R, Preuss TM, Rilling JK, Li L (2015a): Comparison of diffusion tractography and tract-tracing measures of connectivity strength in rhesus macaque connectome. Hum Brain Mapp 36:3064–3075.
72. van den Heuvel MP, Scholtens LH, de Reus MA, Kahn RS (2015b): Associated Microscale Spine Density and Macroscale Connectivity Disruptions in Schizophrenia. Biological psychiatry (Epub ahead of print).
73. van den Heuvel MP, Scholtens LH, Feldman Barrett L, Hilgetag CC, de Reus MA (2015c): Bridging cytoarchitectonics and connectomics in human cerebral cortex. J Neurosci 35:13943–13948.
74. van den Heuvel MP, Bullmore ET, Sporns O (2016): Comparative connectomics. Trends in Cognitive Sciences. 20:345–361.
75. Van Essen DC, Smith SM, Barch DM, Behrens TE, Yacoub E, Ugurbil K (2013): The WU-Minn human connectome project: An overview. NeuroImage 80:62–79.
76. Vanduffel W, Fize D, Mandeville JB, Nelissen K, Van Hecke P, Rosen BR, Tootell RBH, Orban GA (2001): Visual motion processing investigated using contrast agent-enhanced fMRI in awake behaving monkeys. Neuron 32:565–577.
77. von Bonin G, Bailey P (1947): The neocortex of Macaca mulatta. Urbana: Univ. of Illinois Press. Champaign, USA.
78. Walker A (1940): Cytoarchitectural study of the prefrontal area of the macaque monkey. J Comp Neurol 73:27.
79. Zilles K, Amunts K (2009): Receptor mapping: Architecture of the human cerebral cortex. Curr Opin Neurol 22:331–339.
80. Zilles K, Bacha-Trams M, Palomero-Gallagher N, Amunts K, Friederici AD (2015): Common molecular basis of the sentence comprehension network revealed by neurotransmitter receptor fingerprints. Cortex 63:79–89.
81. Zilles K, Palomero-Gallagher N, Grefkes C, Scheperjans F, Boy C, Amunts K, Schleicher A (2002): Architectonics of the human cerebral cortex and transmitter receptor fingerprints: Reconciling functional neuroanatomy and neurochemistry. Eur Neuropsychopharmacol 12:587–599.