BA3b and BA1 activate in a serial fashion after median nerve stimulation: Direct evidence from combining source analysis of evoked fields and cytoarchitectonic probabilistic maps

NeuroImage

Volumn 54, Issue 1, 2011, Pages 60-73

  Papadelis, Christos ^a,b   Eickhoff, Simon B ^c,d,e   Zilles, Karl ^c   Ioannides, Andreas A ^a,f  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b UNIVERSITY OF TRENTO   (Italy)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

^d UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^e Section JARA FIT   (Germany)

^f AAI SCIENTIFIC CULTURAL SERVICES LTD   (Cyprus)

Author keywords

Cytoarchitectonic probabilistic maps; Median nerve; Serial processing; Somatosensory evoked fields

Indexed keywords

ADULT; ARTICLE; BRAIN CORTEX; BRAIN MAPPING; BRODMANN AREA 1; BRODMANN AREA 3B; CONTROLLED STUDY; CYTOARCHITECTURE; DIPOLE; EVOKED CORTICAL RESPONSE; EVOKED SOMATOSENSORY RESPONSE; FEMALE; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; LATENT PERIOD; MAGNETIC FIELD; MAGNETOENCEPHALOGRAPHY; MALE; MEDIAN NERVE; NERVE CONDUCTION; NERVE STIMULATION; NORMAL HUMAN; PRIORITY JOURNAL; PROBABILISTIC CYTOARCHITECTONIC MAP; QUANTITATIVE ANALYSIS; STRUCTURE ANALYSIS;

ADULT; ALGORITHMS; ELECTRIC STIMULATION; ELECTROOCULOGRAPHY; EVOKED POTENTIALS; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; FUNCTIONAL LATERALITY; HAND; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETOENCEPHALOGRAPHY; MALE; MEDIAN NERVE; MONTE CARLO METHOD; PROBABILITY; THUMB; USER-COMPUTER INTERFACE; WRIST;

EID: 77957956302     PISSN: 10538119     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2010.07.054     Document Type: Article

References (99)

1. Allison T., Wood C.C., McCarthy G. Somatosensory evoked potentials following surgical excision of somatosensory or motor cortex in the monkey. Soc. Neurosci. Abstr. 1986, 12:1432.
2. Allison T., McCarthy G., Wood C.C., Jones S.J. Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings. Brain 1991, 114(Pt 6):2465-2503.
3. Allison T., Wood C.C., McCarthy G., Spencer D.D. Cortical somatosensory evoked potentials. II. Effects of excision of somatosensory or motor cortex in humans and monkeys. J. Neurophysiol. 1991, 66(1):64-82.
4. Allison T., McCarthy G., Wood C.C., Darcey T.M., Spencer D.D., Williamson P.D. Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. J. Neurophysiol. 1989, 62(3):694-710.
5. Amiez C., Petrides M. Anatomical organization of the eye fields in the human and non-human primate frontal cortex. Progr. Neurobiol. 2009, 89:220-230.
6. Amunts K., Schleicher A., Bürgel U., Mohlberg H., Uylings H.B.M., Zilles K. Broca's region revisited: cytoarchitecture and intersubject variability. J. Comp. Neurol. 1999, 412:319-341.
7. Amunts K., Malikovic A., Mohlberg H., Schormann T., Zilles K. Brodmann's areas 17 and 18 brought into stereotaxic space - where and how variable?. Neuroimage 2000, 11:66-84.
8. Amunts K., Zilles K. Advances in cytoarchitectonic mapping of the human cerebral cortex. Neuroimaging Clin. N. Am. 2001, 11(2):151-169.
9. Amunts K., Weiss P.H., Mohlberg H., Pieperhoff P., Eickhoff S., Gurd J.M., Marshall J.C., Shah J.N., Fink G.R., Zilles K. Analysis of the neural mechanisms underlying verbal fluency in cytoarchitectonically defined stereotaxic space - the roles of Brodmann areas 44 and 45. Neuroimage 2004, 22:42-56.
10. Ashburner J., Friston K.J. Unified segmentation. Neuroimage 2005, 26(3):839-851.
11. Barnikol U.B., Amunts K., Dammers J., Mohlberg H., Fieseler T., Malikovic A., Zilles K., Niedeggen M., Tass P.A. Pattern reversal visual evoked responses of V1/V2 and V5/MT as revealed by MEG combined with probabilistic cytoarchitectonic maps. Neuroimage 2006, 31(1):86-108.
12. Baumgartner C., Sutherling W.W., Di S., Barth D.S. Spatiotemporal modeling of cerebral evoked magnetic fields to median nerve stimulation. Electroencephalogr. Clin. Neurophysiol. 1991, 79(1):27-35.
13. Binkofski F., Amunts K., Stephan K.M., Posse S., Schormann T., Freund H.J., Zilles K., Seitz R.J. Broca's region subserves imagery of motion: a combined cytoarchitectonic and fMRI study. Hum. Brain Mapp. 2000, 11(4):273-285.
14. Bodegård A., Geyer S., Naito E., Zilles K., Roland P.E. Somatosensory areas in man activated by moving stimuli. Cytoarchitectonic mapping and PET. NeuroReport 2000, 11:187-191.
15. Bodegård A., Geyer S., Herath P., Grefkes C., Zilles K., Roland P.E. Somatosensory areas engaged during discrimination of steady pressure, spring strength and kinaesthesia. Hum. Brain Mapp. 2003, 20:103-115.
16. Brodmann K. Vergleichende Lokalisationslehre der Großhirnrinde 1909, Barth, Leipzig.
17. Buchner H., Fuchs M., Wischmann H.A., Dössel O., Ludwig I., Knepper A., Berg P. Source analysis of median nerve and finger stimulated somatosensory evoked potentials: multichannel simultaneous recording of electric and magnetic fields combined with 3D-MR tomography. Brain Topogr. 1994, 6(4):299-310.
18. Dammers J., Mohlberg H., Boers F., Tass P., Amunts K., Mathiak K. A new toolbox for combining magnetoencephalographic source analysis and cytoarchitectonic probabilistic data for anatomical classification of dynamic brain activity. Neuroimage 2007, 34:1577-1587.
19. Dumoulin S.O., Bittar R.G., Kabani N.J., Baker C.L., Le Goualher G., Bruce Pike G., Evans A.C. A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. Cereb. Cortex 2000, 10(5):454-463.
20. Eickhoff S.B., Stephan K.E., Mohlberg H., Grefkes C., Fink G.R., Amunts K., Zilles K. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 2005, 25(4):1325-1335.
21. Eickhoff S.B., Heim S., Zilles K., Amunts K. Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 2006, 32(2):570-582.
22. Eickhoff S.B., Lotze M., Wietek B., Amunts K., Enck P., Zilles K. Segregation of visceral and somatosensory afferents: an fMRI and cytoarchitectonic mapping study. Neuroimage 2006, 31(3):1004-1014.
23. Eickhoff S.B., Paus T., Caspers S., Grosbras M.H., Evans A., Zilles K., Amunts K. Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 2007, 36(3):511-521.
24. Eickhoff S.B., Grefkes C., Fink G.R., Zilles K. Functional lateralisation of face, hand and trunk representation in anatomically defined human somatosensory areas. Cereb. Cortex 2008, 18:2820-2830.
25. Evans A.C., Marrett S., Neelin P., Collins L., Worsley K., Dai W., Milot S., Meyer E., Bub D. Anatomical mapping of functional activation in stereotactic coordinate space. Neuroimage 1992, 1:43-53.
26. Forss N., Hari R., Salmelin R., Ahonen A., Hämäläinen M., Kajola M., Knuutila J., Simola J. Activation of the human posterior parietal cortex by median nerve stimulation. Exp. Brain Res. 1994, 99(2):309-315.
27. Gardner E.P., Hämäläinen H.A., Warren S., Davis J., Young W. Somatosensory evoked potentials (SEPs) and cortical single unit response elicited by mechanical tactile stimuli in awake monkeys. Electroencephalogr. Clin. Neurophysiol. 1984, 58:537-552.
28. Garraghty P.E., Florence S.L., Kaas J.H. Ablations of areas 3a and 3b of monkey somatosensory cortex abolish cutaneous responsivity in area 1. Brain Res. 1990, 528(1):165-169.
29. Geyer S., Ledberg A., Schleicher A., Kinomura S., Schormann T., Burgel U., Klingberg T., Larsson J., Zilles K., Roland P.E. Two different areas within the primary motor cortex of man. Nature 1996, 382:805-807.
30. Geyer S., Schleicher A., Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex: 1. Microstructural organization and interindividual variability. NeuroImage 1999, 10:63-83.
31. Geyer S., Schormann T., Mohlberg H., Zilles K. Areas 3a, 3b, and 1 of human primary somatosensory cortex. 2. Spatial normalization to standard anatomical space. Neuroimage 2000, 11:684-696.
32. Geyer S., Schleicher A., Schormann T., Mohlberg H., Bodegård A., Roland P.E., Zilles K. Integration of microstructural and functional aspects of human somatosensory areas 3a, 3b, and 1 on the basis of a computerized brain atlas. Anat. Embryol. (Berl) 2001, 204(4):351-366.
33. Grefkes C., Geyer S., Schormann T., Roland P., Zilles K. Human somatosensory area 2: observer-independent cytoarchitectonic mapping, interindividual variability, and population map. Neuroimage 2001, 14:617-631.
34. Gross J., Ioannides A.A. Linear transformations of data space in MEG. Phys. Med. Biol. 1999, 44:2081-2097.
35. Hämäläinen M., Hari R., Ilmoniemi R.J., Knuutila J., Lounasmaa O.V. Magnetoencephalography - theory, instrumentation, and applications to noninvasive studies of the working human brain. Rev. Mod. Phys. 1993, 65(2):413-497.
36. Hari R., Reinikainen K., Kaukoranta E., Hämäläinen M., Ilmoniemi R., Penttinen A., Salminen J., Teszner D. Somatosensory evoked cerebral magnetic fields from SI and SII in man. Electroencephalogr. Clin. Neurophysiol. 1984, 57(3):254-263.
37. Haueisen J., Schack B., Meier T., Curio G., Okada Y. Multiplicity in the high-frequency signals during the short-latency somatosensory evoked cortical activity in humans. Clin. Neurophysiol. 2001, 112(7):1316-1325.
38. Heim S., Alter K., Ischebeck A.K., Amunts K., Eickhoff S.B., Mohlberg H., Zilles K., Yves von Cramon D., Friederici A.D. The role of the left Brodmann's areas 44 and 45 in reading words and pseudowords. Cognit. Brain Res. 2005, 25:982-993.
39. th International Conference on Biomagnetism 2002, 931-933. Berlin, VDE Verlag. H. Nowak, J. Haueisen, F. Giessler, R. Huonker (Eds.).
40. Horwitz B., Amunts K., Bhattarchayya R., Patkin D., Jeffries K., Zilles K., Braun A.R. Activation of Broca's area during the production of spoken and signed language: A combined cytoarchitectonic mapping and PET analysis. Neuropsychologia 2003, 41:1868-1876.
41. Huttunen J. Does the P35m SEF deflection really come from the motor cortex?. Electroencephalogr. Clin. Neurophysiol. 1997, 104(1):101-102.
42. Ioannides A.A. Estimates of 3D brain activity ms by ms from biomagnetic signals: method (MFT), results and their significance. Quantitative and Topological EEG and MEG analysis 1995, 59-68. Universitatsverlag Druckhaus-Maayer GmbH, Jena. E. Eiselt, U. Zwiener, H. Witte (Eds.).
43. Ioannides A.A. Magnetoencephalography as a research tool in neuroscience: State of the art. Neuroscientist 2006, 12:524-544.
44. Ioannides A.A., Bolton J.P.R., Clarke C.J.S. Continuous probabilistic solutions to the biomagnetic inverse problem. Inverse problem 1990, 6:523-542.
45. Ioannides A.A., Hellstrand E., Abraham-Fuchs K. Point and distributed current density analysis of interictal epileptic activity recorded by magnetoencephalography. Physiol. Meas. 1993, 14:121-130.
46. Ioannides A.A., Singh K.D., Hasson R., Baumann S.B., Rogers R.L., Guinto F.C., Papanicolaou A.C. Comparison of current dipole and magnetic field tomography analyses of the cortical response to auditory stimuli. Brain Topogr. 1993, 6:27-34.
47. Ioannides A.A., Kostopoulos G.K., Laskaris N.A., Liu L.C., Shibata T., Schellens M., Poghosyan V., Khurshudyan A. Timing and connectivity in the human somatosensory cortex from single trial mass electrical activity. Hum. Brain Mapp. 2002, 15:231-246.
48. Inui K., Wang X., Tamura Y., Kaneoke Y., Kakigi R. Serial processing in the human somatosensory system. Cereb. Cortex 2004, 14(8):851-857.
49. Jakobs O., Wang L.E., Dafotakis M., Grefkes C., Zilles K., Eickhoff S.B. Effects of timing and movement uncertainty implicate the temporo-parietal junction in the prediction of forthcoming motor actions. Neuroimage 2009, 47(2):667-677.
50. Jones E.G., Powell T.P.S. Connexions of the somatic sensory cortex of the rhesus monkey. III. Thalamic connexions. Brain 1970, 93:37-56.
51. Kakigi R. Somatosensory evoked magnetic fields following median nerve stimulation. Neurosci. Res. 1994, 20(2):165-174.
52. Karhu J., Tesche C.D. Simultaneous early processing of sensory input in human primary (SI) and secondary (SII) somatosensory cortices. J. Neurophysiol. 1999, 81(5):2017-2025.
53. Kawamura T., Nakasato N., Seki K., Kanno A., Fujita S., Fujiwara S., Yoshimoto T. Neuromagnetic evidence of pre- and post-central cortical sources of somatosensory evoked responses. Electroencephalogr. Clin. Neurophysiol. 1996, 100(1):44-50.
54. Kimura T., Ozaki I., Hashimoto I. Impulse propagation along thalamocortical fibers can be detected magnetically outside the human brain. J. Neurosci. 2008, 28(47):12535-12538.
55. Korvenoja A., Wikstrom H., Huttunen J., Virtanan J., Laine P., Aronen H.J., Seppalainen A.M., Ilmoniemi R.J. Activation of ipsilateral primary sensorimotor cortex by median nerve stimulation. NeuroReport 1995, 6(18):2589-2593.
56. Laskaris N.A., Ioannides A.A. Exploratory data analysis of evoked response single trials based on minimal spanning tree. Clin. Neurophysiol. 2001, 112(4):698-712.
57. Laskaris N.A., Liu L.C., Ioannides A.A. Single-trial variability in early visual neuromagnetic responses: an explorative study based on the regional activation contributing to the N70m peak. Neuroimage 2003, 20(2):765-783.
58. Leahy R.M., Mosher J.C., Spencer M.E., Huang M.X., Lewine J.D. A study of dipole localization accuracy for MEG and EEG using a human skull phantom. Electroencephalogr. Clin. Neurophysiol. 1998, 107(2):159-173.
59. Lee T.W., Girolami M., Sejnowski T.J. Independent component analysis using an extended INFOMAX algorithm for mixed sub-Gaussian and super-Gaussian sources. Neural Comput. 1999, 11:606-633.
60. Liu L.C., Ioannides A.A., Mueller-Gaertner H.W. Bi-hemispheric study of single trial MEG signals of the human auditory cortex. Electroenceph. Clin. Neurophysiol 1998, 106:64-78.
61. Mauguière F., Merlet I., Forss N., Vanni S., Jousmäki V., Adeleine P., Hari R. Activation of a distributed somatosensory cortical network in the human brain. A dipole modelling study of magnetic fields evoked by median nerve stimulation. Part I: Location and activation timing of SEF sources. Electroencephalogr. Clin. Neurophysiol. 1997, 104(4):281-289.
62. McCarthy G., Wood C.C., Allison T. Cortical somatosensory evoked potentials. I. Recordings in the monkey Macaca fascicularis. J. Neurophysiol. 1991, 66(1):53-63.
63. Mima T., Nagamine T., Nishitani N., Mikuni N., Ikeda A., Fukuyama H., Takigawa T., Kimura J., Shibasaki H. Cortical myoclonus: sensorimotor hyperexcitability. Neurology 1998, 50(4):933-942.
64. Mitzdorf U. Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol. Rev. 1985, 65:37-100.
65. Mohlberg H., Lerch J., Amunts K., Evans A.C., Zilles K. Probabilistic cytoarchitectonic maps transformed into MNI space. NeuroImage 2003, 19(2). Academic Press, San Diego.
66. Moradi F., Liu L.C., Cheng K., Waggoner R.A., Tanaka K., Ioannides A.A. Consistent and precise localization of brain activity in human primary visual cortex by MEG and fMRI. Neuroimage 2003, 18(3):595-609.
67. Papadelis C., Poghosyan V., Fenwick P.B., Ioannides A.A. MEG's ability to localise accurately weak transient neural sources. Clin. Neurophysiol. 2009, 120(11):1958-1970.
68. Papadelis C., Poghosyan V., Ioannides A.A. Phantom study supports claim of accurate localization from MEG data. Int. J. Bioelectromagnetism 2007, 9(3):163-167.
69. Papakostopoulos D., Crow H.J. Direct recording of the somatosensory evoked potentials from the cerebral cortex of man and the difference between precentral and postcentral potentials. Progr Clin Neurophysiol 1980, vol. 7:15-26. Basel, Karger. J.E. Desmedt (Ed.).
70. Phillips J.W., Leahy R.M., Mosher J.C. MEG-based imaging of focal neuronal current sources. IEEE Trans. Med. Imaging 1997, 16:338-348.
71. Poghosyan V., Ioannides A.A. Attention modulates earliest responses in the primary auditory and visual cortices. Neuron 2008, 58:802-813.
72. Powell T.P.S., Mountcastle V.B. The cytoarchitecture of the postcentral gyrus of the monkey Macaca mulatta. Bull. Johns Hopkins Hosp. 1959, 105:108-131.
73. Prieto E.A., Barnikol U.B., Soler E.P., Dolan K., Hesselmann G., Mohlberg H., Amunts K., Zilles K., Niedeggen M., Tass P.A. Timing of V1/V2 and V5+ activations during coherent motion of dots: an MEG study. Neuroimage 2007, 37(4):1384-1395.
74. Rossini P.M., Deuschl G., Pizzella V., Tecchio F., Pasquarelli A., Feifel E., Romani G.L., Lücking C.H. Topography and sources of electromagnetic cerebral responses to electrical and air-puff stimulation of the hand. Electroencephalogr. Clin. Neurophysiol. 1996, 100(3):229-239.
75. Schlag J. Generation of brain evoked potentials. Cellular Processes and Brain Potentials, New York: Academic, part. A 1973, 273-316. R.F. Thompson, M.M. Patterson (Eds.).
76. Schleicher A., Palomero-Gallagher N., Morosan P., Eickhoff S.B., Kowalski T., de Vos K., Amunts K., Zilles K. Quantitative architectural analysis: a new approach to cortical mapping. Anat. Embryol. (Berl) 2005, 210(5-6):373-386.
77. Stohr P.E., Goldring S. Origin of somatosensory evoked scalp responses in man. J. Neurosurg. 1969, 31:117-127.
78. Taylor J.G., Ioannides A.A., Muller-Gartner H.W. Mathematical analysis of lead field expansions. IEEE Trans. Med. Imaging 1999, 18:151-163.
79. Tecchio F., Pasqualetti P., Pizzella V., Romani G., Rossini P.M. Morphology of somatosensory evoked fields: inter-hemispheric similarity as a parameter for physiological and pathological neural connectivity. Neurosci. Lett. 2000, 287(3):203-206.
80. Tecchio F., Rossini P.M., Pizzella V., Cassetta E., Romani G.L. Spatial properties and interhemispheric differences of the sensory hand cortical representation: a neuromagnetic study. Brain Res. 1997, 767(1):100-108.
81. Tesche C.D., Karhu J. Somatosensory evoked magnetic fields arising from sources in the human cerebellum. Brain Res. 1997, 744(1):23-31.
82. Tiihonen J., Hari R., Hämäläinen M. Early deflections of cerebral magnetic responses to median nerve stimulation. Electroencephalogr. Clin. Neurophysiol. 1989, 74(4):290-296.
83. Tootell R.B., Reppas J.B., Kwong K.K., Malach R., Born R.T., Brady T.J., Rosen B.R., Belliveau J.W. Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging. J. Neurosci. 1995, 15(4):3215-3230.
84. Towe A.L. On the nature of the primary evoked response. Exp. Neurol. 1966, 15:113-139.
85. Vates G.E., Lawton M.T., Wilson C.B., McDermott M.W., Halbach V.V., Roberts T.P., Rowley H.A. Magnetic source imaging demonstrates altered cortical distribution of function in patients with arteriovenous malformations. Neurosurgery 2002, 51(3):614-623.
86. Vogt B.A., Pandya D.N. Cortico-cortical connections of somatic sensory cortex (areas 3, 1 and 2) in the rhesus monkey. J. Comp. Neurol. 1978, 177(2):179-191.
87. Wikström H., Huttunen J., Korvenoja A., Virtanen J., Salonen O., Aronen H., Ilmoniemi R.J. Effects of interstimulus interval on somatosensory evoked magnetic fields (SEFs): a hypothesis concerning SEF generation at the primary sensorimotor cortex. Electroencephalogr. Clin. Neurophysiol. 1996, 100(6):479-487.
88. Wilms M., Eickhoff S.B., Specht K., Amunts K., Shah N.J., Malikovic A., Fink G.R. Human V5/MT+: comparison of functional and cytoarchitectonic data. Anat. Embryol. (Berl) 2005, 210:485-495.
89. Wilms M., Eickhoff S.B., Hömke L., Rottschy C., Kujovic M., Amunts K., Fink G.R. Comparison of functional and cytoarchitectonic maps of human visual areas V1, V2, V3d, V3v, and V4(v). Neuroimage 2010, 49(2):1171-1179.
90. Wohlschläger A.M., Specht K., Lie C.-H., Mohlberg H., Wohlschläger A., Bente K., Pietrzyk U., Stöcker T., Zilles K., Amunts K., Fink G.R. Linking retinotopic fMRI mapping and anatomical probability maps of human occipital areas V1 and V2. Neuroimage 2005, 26:73-82.
91. Wood C.C., Cohen D., Cuffin B.N., Yarita M., Allison T. Electrical sources in human somatosensory cortex: identification by combined magnetic and potential recordings. Science 1985, 227(4690):1051-1053.
92. Wood C.C., Allison T., McCarthy G., Spencer D.D., Williamson P.D. Somatosensory evoked potentials following surgical excision of human somatosensory or motor cortex. Soc. Neurosci. Abstr. 1986, 12:1432.
93. Wood C.C., Spencer D.D., Allison T., McCarthy G., Williamson P.D., Goff W.R. Localization of human sensorimotor cortex during surgery by cortical surface recording of somatosensory evoked potentials. J. Neurosurg. 1988, 68(1):99-111.
94. Wunderlich G., Knorr U., Herzog H., Kiwit J.C., Freund H.J., Seitz R.J. Precentral glioma location determines the displacement of cortical hand representation. Neurosurgery 1998, 42(1):18-26.
95. Yang T.T., Gallen C.C., Schwartz B.J., Bloom F.E. Noninvasive somatosensory homunculus mapping in humans by using a large-array biomagnetometer. Proc. Natl Acad. Sci. 1993, 90(7):3098-3102.
96. Young J.P., Geyer S., Grefkes C., Amunts K., Morosan P., Zilles K., Roland P.E. Regional cerebral blood flow correlations of somatosensory areas 3a, 3b, 1, and 2 in humans during rest: A PET and cytoarchitectural study. Hum. Brain Mapp. 2003, 19:183-196.
97. Zeki S., Watson J.D., Lueck C.J., Friston K.J., Kennard C., Frackowiak R.S. A direct demonstration of functional specialization in human visual cortex. J. Neurosci. 1991, 11(3):641-649.
98. Zilles, K., Schleicher, A., Palomero-Gallagher, N., Amunts, K., 2002. Quantitative analysis of cyto- and receptor architecture of the human brain. In: Mazziotta, J., Toga, A. (Eds.), Brain Mapping, the Methods, Elsevier, pp. 573-602.
99. Zilles K., Amunts K. Centenary of Brodmann's map - conception and fate. Nat. Rev. Neurosci. 2010, 11(2):139-145.