Spatiotemporal dynamics of bimanual integration in human somatosensory cortex and their relevance to bimanual object manipulation

Journal of Neuroscience

Volumn 32, Issue 16, 2012, Pages 5667-5677

  Jung, Patrick ^a,b   Klein, Johannes C ^a   Wibral, Michael ^a   Hoechstetter, Karsten ^d   Bliem, Barbara ^a   Lu, Ming Kuei ^a,c   Wahl, Mathias ^a   Ziemann, Ulf ^a  

^a GOETHE UNIVERSITY   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c CHINA MEDICAL UNIVERSITY HOSPITAL   (Taiwan)

^d NONE

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; CONDITIONING; CORPUS CALLOSUM; DIFFUSION TENSOR IMAGING; EXPLORATORY BEHAVIOR; FEMALE; FRACTIONAL ANISOTROPY; HUMAN; HUMAN EXPERIMENT; LEFT HEMISPHERE; MAGNETOENCEPHALOGRAPHY; MALE; MEDIAN NERVE; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OBJECT MANIPULATION; POSTERIOR PARIETAL CORTEX; PREMOTOR CORTEX; PRIMARY SOMATOSENSORY CORTEX; PRIORITY JOURNAL; RIGHT HEMISPHERE; SECONDARY SOMATOSENSORY CORTEX; SENSORIMOTOR INTEGRATION; SOMATOSENSORY CORTEX; STIMULUS; TACTILE DISCRIMINATION; TASK PERFORMANCE;

ADULT; ANALYSIS OF VARIANCE; BRAIN MAPPING; CORPUS CALLOSUM; ELECTRIC STIMULATION; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, SOMATOSENSORY; FEMALE; FUNCTIONAL LATERALITY; HAND; HUMANS; MAGNETIC RESONANCE IMAGING; MAGNETOENCEPHALOGRAPHY; MALE; MEDIAN NERVE; PHOTIC STIMULATION; PROBABILITY; PSYCHOMOTOR PERFORMANCE; SOMATOSENSORY CORTEX; TOUCH; WRIST; YOUNG ADULT;

EID: 84859738631     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/jneurosci.5957-11.2012     Document Type: Article

References (76)

1. Aboitiz F, Scheibel AB, Fisher RS, Zaidel E (1992) Fiber composition of the human corpus callosum. Brain Res 598:143-153.
2. Aglioti S, Beltramello A, Tassinari G, Berlucchi G (1998) Paradoxically greater interhemispheric transfer deficits in partial than complete callosal agenesis. Neuropsychologia 36:1015-1024.
3. Allison T, McCarthy G, Wood CC, Darcey TM, Spencer DD, Williamson PD (1989a) Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity. J Neurophysiol 62:694-710.
4. Allison T, McCarthy G, Wood CC, Williamson PD, Spencer DD (1989b) Human cortical potentials evoked by stimulation of the median nerve. II. Cytoarchitectonic areas generating long-latency activity. J Neurophysiol 62:711-722.
5. Allison T, McCarthy G, Wood CC (1992) The relationship between human long-latency somatosensory evoked potentials recorded from the cortical surface and from the scalp. Electroencephalogr Clin Neurophysiol 84:301-314.
6. Behrens TE, Woolrich MW, Jenkinson M, Johansen-Berg H, Nunes RG, Clare S, Matthews PM, Brady JM, Smith SM (2003) Characterization and propagation of uncertainty in diffusion-weighted MR imaging. Magn Reson Med 50:1077-1088.
7. Behrens TE, Berg HJ, Jbabdi S, Rushworth MF, Woolrich MW (2007) Probabilistic diffusion tractography with multiple fibre orientations: what can we gain? Neuroimage 34:144-155.
8. Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Eshel N, Josephs O, Weiskopf N, Driver J (2008) Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI. J Neurosci 28:13202-13208.
9. Disbrow E, Roberts T, Krubitzer L (2000) Somatotopic organization of cortical fields in the lateral sulcus of Homo sapiens: evidence for SII and PV. J Comp Neurol 418:1-21.
10. Efron B, Tibshirani RJ (1993) An introduction to the bootstrap. New York: Chapman and Hall.
11. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325-1335.
12. Eickhoff SB, Schleicher A, Zilles K, Amunts K (2006) The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions. Cereb Cortex 16:254-267.
13. Eickhoff SB, Grefkes C, Fink GR, Zilles K (2008) Functional lateralization of face, hand, and trunk representation in anatomically defined human somatosensory areas. Cereb Cortex 18:2820-2830.
14. Eickhoff SB, Jbabdi S, Caspers S, Laird AR, Fox PT, Zilles K, Behrens TE (2010) Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum. J Neurosci 30:6409-6421.
15. Fabri M, Polonara G, Quattrini A, Salvolini U, Del Pesce M, Manzoni T (1999) Role of the corpus callosum in the somatosensory activation of the ipsilateral cerebral cortex: an fMRI study of callosotomized patients. Eur J Neurosci 11:3983-3994.
16. Fabri M, Polonara G, Del Pesce M, Quattrini A, Salvolini U, Manzoni T (2001) Posterior corpus callosum and interhemispheric transfer of somatosensory information: an fMRI and neuropsychological study of a partially callosotomized patient. J Cogn Neurosci 13:1071-1079.
17. Fabri M, Del Pesce M, Paggi A, Polonara G, Bartolini M, Salvolini U, Manzoni T (2005) Contribution of posterior corpus callosum to the interhemispheric transfer of tactile information. Brain Res Cogn Brain Res 24:73-80.
18. Ferbert A, Priori A, Rothwell JC, Day BL, Colebatch JG, Marsden CD (1992) Interhemispheric inhibition of the human motor cortex. J Physiol 453:525-546.
19. Fitzgerald PJ, Lane JW, Thakur PH, Hsiao SS (2006) Receptive field (RF) properties of the macaque second somatosensory cortex: RF size, shape, and somatotopic organization. J Neurosci 26:6485-6495.
20. Forss N, Hari R, Salmelin R, Ahonen A, Hämäläinen M, Kajola M, Knuutila J, Simola J (1994) Activation of the human posterior parietal cortex by median nerve stimulation. Exp Brain Res 99:309-315.
21. Forss N, Hietanen M, Salonen O, Hari R (1999) Modified activation of somatosensory cortical network in patients with right-hemisphere stroke. Brain 122:1889-1899.
22. Frot M, Magnin M, Mauguiére F, Garcia-Larrea L (2007) Human SII and posterior insula differently encode thermal laser stimuli. Cereb Cortex 17:610-620.
23. Gardner EP, Costanzo RM (1980) Temporal integration of multiple-point stimuli in primary somatosensory cortical receptive fields of alert monkeys. J Neurophysiol 43:444-468.
24. Gazzaniga MS, Freedman H (1973) Observations on visual processes after posterior callosal section. Neurology 23:1126-1130.
25. Geyer S (2003) The microstructural border between the motor and the cognitive domain in the human cerebral cortex. Vienna: Springer.
26. Geyer S, Schleicher A, Zilles K (1999) Areas 3a, 3b, and 1 of human primary somatosensory cortex. Neuroimage 10:63-83.
27. Greenwood PM, Goff WR (1987) Modification of median nerve somatic evoked potentials by prior median nerve, peroneal nerve, and auditory stimulation. Electroencephalogr Clin Neurophysiol 68:295-302.
28. Hari R, Forss N (1999) Magnetoencephalography in the study of human somatosensory cortical processing. Philos Trans R Soc Lond B Biol Sci 354:1145-1154.
29. Hinkley LB, Krubitzer LA, Nagarajan SS, Disbrow EA (2007) Sensorimotor integration in S2, PV, and parietal rostroventral areas of the human sylvian fissure. J Neurophysiol 97:1288-1297.
30. Hlushchuk Y, Hari R (2006) Transient suppression of ipsilateral primary somatosensory cortex during tactile finger stimulation. J Neurosci 26:5819-5824.
31. Hoechstetter K, Rupp A, Stancák A, Meinck HM, Stippich C, Berg P, Scherg M (2001) Interaction of tactile input in the human primary and secondary somatosensory cortex-a magnetoencephalographic study. Neuroimage 14:759-767.
32. Hübers A, Orekhov Y, Ziemann U (2008) Interhemispheric motor inhibition: its role in controlling electromyographic mirror activity. Eur J Neurosci 28:364-371.
33. Huttunen J, Ahlfors S, Hari R (1992) Interaction of afferent impulses in the human primary sensorimotor cortex. Electroencephalogr Clin Neurophysiol 82:176-181.
34. Iwamura Y (2000) Bilateral receptive field neurons and callosal connections in the somatosensory cortex. Philos Trans R Soc Lond B Biol Sci 355:267-273.
35. Iwamura Y, Taoka M, Iriki A (2001) Bilateral activity and callosal connections in the somatosensory cortex. Neuroscientist 7:419-429.
36. Jenkinson M, Smith S (2001) A global optimisation method for robust affine registration of brain images. Med Image Anal 5:143-156.
37. Jenkinson M, Bannister P, Brady M, Smith S (2002) Improved optimization for the robust and accurate linear registration and motion correction of brain images. Neuroimage 17:825-841.
38. Johansson RS, Flanagan JR (2009) Coding and use of tactile signals from the fingertips in object manipulation tasks. Nat Rev Neurosci 10:345-359.
39. Jones EG, Powell TP (1969) Connexions of the somatic sensory cortex of the rhesus monkey. II. Contralateral cortical connexions. Brain 92:717-730.
40. Jung P, Baumgärtner U, Magerl W, Treede RD (2008) Hemispheric asymmetry of hand representation in human primary somatosensory cortex and handedness. Clin Neurophysiol 119:2579-2586.
41. Jung P, Baumgärtner U, Stoeter P, Treede RD (2009) Structural and functional asymmetry in the human parietal opercular cortex. J Neurophysiol 101:3246-3257.
42. Kanno A, Nakasato N, Hatanaka K, Yoshimoto T (2003) Ipsilateral area 3b responses to median nerve somatosensory stimulation. Neuroimage 18:169-177.
43. Kastrup A, Baudewig J, Schnaudigel S, Huonker R, Becker L, Sohns JM, Dechent P, Klingner C, Witte OW (2008) Behavioral correlates of negative BOLD signal changes in the primary somatosensory cortex. Neuroimage 41:1364-1371.
44. Killackey HP, Gould HJ 3rd, Cusick CG, Pons TP, Kaas JH (1983) The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys. J Comp Neurol 219:384-419.
45. Klingner CM, Huonker R, Flemming S, Hasler C, Brodoehl S, Preul C, Burmeister H, Kastrup A, Witte OW (2011) Functional deactivations: multiple ipsilateral brain areas engaged in the processing of somatosensory information. Hum Brain Mapp 32:127-140.
46. Koch G, Cercignani M, Bonnì S, Giacobbe V, Bucchi G, Versace V, Caltagirone C, Bozzali M (2011) Asymmetry of parietal interhemispheric connections in humans. J Neurosci 31:8967-8975.
47. Krubitzer LA, Kaas JH (1990) The organization and connections of somatosensory cortex in marmosets. J Neurosci 10:952-974.
48. Le Bihan D (2003) Looking into the functional architecture of the brain with diffusion MRI. Nat Rev Neurosci 4:469-480.
49. Liu H, Schimpf PH, Dong G, Gao X, Yang F, Gao S (2005) Standardized shrinking LORETA-FOCUSS (SSLOFO): a new algorithm for spatiotemporal EEG source reconstruction. IEEE Trans Biomed Eng 52:1681-1691.
50. Manzoni T, Conti F, Fabri M (1986) Callosal projections from area SII to SI in monkeys: anatomical organization and comparison with association projections. J Comp Neurol 252:245-263.
51. Mauguiére F, Merlet I, Forss N, Vanni S, Jousmäki V, Adeleine P, Hari R (1997) 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 104:281-289.
52. Mima T, Ikeda A, Nagamine T, Yazawa S, Kunieda T, Mikuni N, Taki W, Kimura J, Shibasaki H (1997) Human second somatosensory area: subdural and magnetoencephalographic recording of somatosensory evoked responses. J Neurol Neurosurg Psychiatry 63:501-505.
53. Nihashi T, Naganawa S, Sato C, Kawai H, Nakamura T, Fukatsu H, Ishigaki T, Aoki I (2005) Contralateral and ipsilateral responses in primary somatosensory cortex following electrical median nerve stimulation-an fMRI study. Clin Neurophysiol 116:842-848.
54. Oldfield RC (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 9:97-113.
55. Pandya DN, Vignolo LA (1968) Interhemispheric neocortical projections of somatosensory areas I and II in the rhesus monkey. Brain Res 7:300-303.
56. Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24 Suppl D:5-12.
57. Ploner M, Schmitz F, Freund HJ, Schnitzler A (2000) Differential organization of touch and pain in human primary somatosensory cortex. J Neurophysiol 83:1770-1776.
58. Ragert P, Nierhaus T, Cohen LG, Villringer A (2011) Interhemispheric interactions between the human primary somatosensory cortices. PLoS One 6:e16150.
59. Reed JL, Qi HX, Kaas JH (2011) Spatiotemporal properties of neuron response suppression in owl monkey primary somatosensory cortex when stimuli are presented to both hands. J Neurosci 31:3589-3601.
60. Robinson CJ, Burton H (1980) Organization of somatosensory receptive fields in cortical areas 7b, retroinsula, postauditory and granular insula of M. fascicularis. J Comp Neurol 192:69-92.
61. Sauerwein HC, Lassonde M (1997) Neuropsychological alterations after split-brain surgery. J Neurosurg Sci 41:59-66.
62. Scheperjans F, Hermann K, Eickhoff SB, Amunts K, Schleicher A, Zilles K (2008) Observer-independent cytoarchitectonic mapping of the human superior parietal cortex. Cereb Cortex 18:846-867.
63. Scherg M (1990) Fundamentals of dipole source potential analysis. In: Auditory evoked magnetic fields and electric potentials (Grandori F, Hoke M, Romani GL, eds), pp 40-69. Basel: Karger.
64. Simões C, Hari R (1999) Relationship between responses to contra-and ipsilateral stimuli in the human second somatosensory cortex SII. Neuroimage 10:408-416.
65. Smith SM (2002) Fast robust automated brain extraction. Hum. Brain Mapp 17:143-155.
66. Stancák A Jr, Lücking CH, Kristeva-Feige R (2000) Lateralization of movement-related potentials and the size of corpus callosum. Neuroreport 11:329-332.
67. Stancák A, Polácek H, Vrána J, Rachmanová R, Hoechstetter K, Tintra J, Scherg M (2005) EEG source analysis and fMRI reveal two electrical sources in the fronto-parietal operculum during subepidermal finger stimulation. Neuroimage 25:8-20.
68. Sutherland MT, Tang AC (2006) Reliable detection of bilateral activation in human primary somatosensory cortex by unilateral median nerve stimulation. Neuroimage 33:1042-1054.
69. Swinnen SP (2002) Intermanual coordination: from behavioural principles to neural-network interactions. Nat Rev Neurosci 3:348-359.
70. Tecchio F, Rossini PM, Pizzella V, Cassetta E, Romani GL (1997) Spatial properties and interhemispheric differences of the sensory hand cortical representation: a neuromagnetic study. Brain Res 767:100-108.
71. Tomasch J (1954) Size, distribution, and number of fibres in the human corpus callosum. Anat Rec 119:119-135.
72. Tommerdahl M, Simons SB, Chiu JS, Favorov O, Whitsel BL (2006) Ipsilateral input modifies the primary somatosensory cortex response to contralateral skin flutter. J Neurosci 26:5970-5977.
73. Uttal WR, Cook L (1964) Systematics of the evoked somatosensory cortical potential: a psychophysical-electrophysiological comparison. Ann N Y Acad Sci 112:60-80.
74. Wegner K, Forss N, Salenius S (2000) Characteristics of the human contraversus ipsilateral SII cortex. Clin Neurophysiol 111:894-900.
75. Wibral M, Bledowski C, Kohler A, Singer W, Muckli L (2009) The timing of feedback to early visual cortex in the perception of long-range apparent motion. Cereb Cortex 19:1567-1582.
76. Zarei M, Johansen-Berg H, Smith S, Ciccarelli O, Thompson AJ, Matthews PM (2006) Functional anatomy of interhemispheric cortical connections in the human brain. J Anat 209:311-320.