Imaging the neural mechanisms of TMS neglect-like bias in healthy volunteers with the interleaved TMS/fMRI technique: Preliminary evidence

Frontiers in Human Neuroscience

Volumn , Issue NOVEMBER 2012, 2012, Pages

  Ricci, Raffaella ^a,c   Salatino, Adriana ^a,c   Li, Xingbao ^a,b   Funk, Agnes P ^a   Logan, Sarah L ^a   Mu, Qiwen ^a   Johnson, Kevin A ^a,d   Bohning, Daryl E ^b   George, Mark S ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF TURIN   (Italy)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

FMRI; Neglect; Spatial attention; TMS; Visuospatial orienting

Indexed keywords

VITAMIN B GROUP;

ADULT; ANATOMICAL CONCEPTS; ANGULAR GYRUS; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; BRAIN MAPPING; DECISION MAKING; ECHO PLANAR IMAGING; FEASIBILITY STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; HUMAN EXPERIMENT; IMAGE ANALYSIS; IMAGE PROCESSING; INFORMATION PROCESSING; INTRAPARIETAL SULCUS; MIDDLE FRONTAL GYRUS; NORMAL HUMAN; PERCEPTION; POSTERIOR PARIETAL CORTEX; SIGNAL TRANSDUCTION; SUPERIOR FRONTAL GYRUS; SUPERIOR PARIETAL LOBULE; SUPRAMARGINAL GYRUS; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL DEPRIVATION;

EID: 84933680125     PISSN: 16625161     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnhum.2012.00326     Document Type: Article

References (57)

1. Bartolomeo, P. (2006). A parietofrontal network for spatial awareness in the right hemisphere of the human brain. Arch Neurol 63, 1238-1241.
2. Bartolomeo, P., Thiebaut De Schotten, M., and Doricchi, F. (2007). Left unilateral neglect as a disconnection syndrome. Cerebral Cortex 17, 2479-2490.
3. Bestmann, S., Baudewig, J., Siebner, H.R., Rothwell, J.C., and Frahm, J. (2003). Subthreshold high-frequency TMS of human primary motor cortex modulates interconnected frontal motor areas as detected by interleaved fMRI-TMS. Neuroimage 20, 1685-1696.
4. Bestmann, S., Baudewig, J., Siebner, H.R., Rothwell, J.C., and Frahm, J. (2004). Functional MRI of the immediate impact of transcranial magnetic stimulation on cortical and subcortical motor circuits. Eur J Neurosci 19, 1950-1962.
5. Bestmann, S., Ruff, C.C., Blankenburg, F., Weiskopf, N., Driver, J., and Rothwell, J.C. (2008). Mapping causal interregional influences with concurrent TMS-fMRI. Exp Brain Res 191, 383-402.
6. Bisiach, E., and Berti, A. (1995). Consciousness in dyschiria, in The Cognitive Neurosciences, ed. M.S. Gazzaniga. (Cambridge, U.S.A.: MIT Press), 1131-1340.
7. Bisiach, E., Ricci, R., Berruti, G., Genero, R., Pepi, R., and Fumelli, T. (1999). Two-dimensional distortion of space representation in unilateral neglect: perceptual and response-related factors. Neuropsychologia 37, 1491-1498.
8. Bisiach, E., Ricci, R., Lualdi, M., and Colombo, M.R. (1998). Perceptual and response bias in unilateral neglect: two modified versions of the milner landmark task. Brain and Cognition 37, 369-386.
9. Bjoertomt, O., Cowey, A., and Walsh, V. (2002). Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation. Brain 125, 2012-2022.
10. Bjoertomt, O., Cowey, A., and Walsh, V. (2009). Near space functioning of the human angular and supramarginal gyri. J Neuropsychol 3, 31-43.
11. Blankenburg, F., Ruff, C.C., Bestmann, S., Bjoertomt, O., Eshel, N., Josephs, O., Weiskopf, N., and Driver, J. (2008). Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI. J Neurosci 28, 13202-13208.
12. Blankenburg, F., Ruff, C.C., Bestmann, S., Bjoertomt, O., Josephs, O., Deichmann, R., and Driver, J. (2010). Studying the role of human parietal cortex in visuospatial attention with concurrent TMS-fMRI. Cereb Cortex 20, 2702-2711.
13. Bohning, D.E., Shastri, A., Mcgavin, L., Mcconnell, K.A., Nahas, Z., Lorberbaum, J.P., Roberts, D.R., and George, M.S. (2000). Motor cortex brain activity induced by 1-Hz transcranial magnetic stimulation is similar in location and level to that for volitional movement. Invest Radiol 35, 676-683.
14. Brighina, F., Bisiach, E., Oliveri, M., Piazza, A., La Bua, V., Daniele, O., and Fierro, B. (2003). 1Hz repetitive transcranial magnetic stimulation of the unaffected hemisphere ameliorates contralesional visuospatial neglect in humans. Neurosci Lett 336, 131-133.
15. Brighina, F., Bisiach, E., Piazza, A., Oliveri, M., La Bua, V., Daniele, O., and Fierro, B. (2002). Perceptual and response bias in visuospatial neglect due to frontal and parietal repetitive transcranial magnetic stimulation in normal subjects. Neuroreport 13, 2571-2575.
16. Catani, M., Allin, M.P., Husain, M., Pugliese, L., Mesulam, M.M., Murray, R.M., and Jones, D.K. (2007). Symmetries in human brain language pathways correlate with verbal recall. Proc Natl Acad Sci U S A 104, 17163-17168.
17. Chica, A.B., Bartolomeo, P., and Valero-Cabre, A. (2011). Dorsal and ventral parietal contributions to spatial orienting in the human brain. J Neurosci 31, 8143-8149.
18. Corbetta, M., Kincade, M.J., Lewis, C., Snyder, A.Z., and Sapir, A. (2005). Neural basis and recovery of spatial attention deficits in spatial neglect. Nature Neuroscience 8, 1603-1610.
19. Corbetta, M., and Shulman, G.L. (2002). Control of goal-directed and stimulus-driven attention in the brain. Nat Rev Neurosci 3, 201-215.
20. Coslett, H.B., Bowers, D., Fitzpatrick, E., Haws, B., and Heilman, K.M. (1990). Directional hypokinesia and hemispatial inattention in neglect. Brain 113 (Pt 2), 475-486.
21. Doricchi, F., Thiebaut De Schotten, M., Tomaiuolo, F., and Bartolomeo, P. (2008). White matter (dis)connections and gray matter (dys)functions in visual neglect: gaining insights into the brain networks of spatial awareness. Cortex 44, 983-995.
22. Doricchi, F., and Tomaiuolo, F. (2003). The anatomy of neglect without hemianopia: a key role for parietal-frontal disconnection? Neuroreport 14, 2239-2243.
23. Driver, J., Blankenburg, F., Bestmann, S., and Ruff, C.C. (2010). New approaches to the study of human brain networks underlying spatial attention and related processes. Exp Brain Res 206, 153-162.
24. Ellison, A., Schindler, I., Pattison, L.L., and Milner, A.D. (2004). An exploration of the role of the superior temporal gyrus in visual search and spatial perception using TMS. Brain 127, 2307-2315.
25. Fierro, B., Brighina, F., Giglia, G., Palermo, A., Francolini, M., and Scalia, S. (2006). Paired pulse TMS over the right posterior parietal cortex modulates visuospatial perception. J Neurol Sci 247, 144-148.
26. Fierro, B., Brighina, F., Oliveri, M., Piazza, A., La Bua, V., Buffa, D., and Bisiach, E. (2000). Contralateral neglect induced by right posterior parietal rTMS in healthy subjects. Neuroreport 11, 1519-1521.
27. Fierro, B., Brighina, F., Piazza, A., Oliveri, M., and Bisiach, E. (2001). Timing of right parietal and frontal cortex activity in visuo-spatial perception: a TMS study in normal individuals. Neuroreport 12, 2605-2607.
28. Fink, G.R., Marshall, J.C., Shah, N.J., Weiss, P.H., Halligan, P.W., Grosse-Ruyken, M., Ziemons, K., Zilles, K., and Freund, H.J. (2000). Line bisection judgments implicate right parietal cortex and cerebellum as assessed by fMRI. Neurology 54, 1324-1331.
29. Friston, K.J., Holmes, A., Poline, J.B., Price, C.J., and Frith, C.D. (1996). Detecting activations in PET and fMRI: levels of inference and power. Neuroimage 4, 223-235.
30. He, B.J., Snyder, A.Z., Vincent, J.L., Epstein, A., Shulman, G.L., and Corbetta, M. (2007). Breakdown of functional connectivity in frontoparietal networks underlies behavioral deficits in spatial neglect. Neuron 53, 905-918.
31. Heilman, K.M., and Valenstein, E. (1972). Frontal lobe neglect in man. Neurology 22, 660-664.
32. Heinen, K., Ruff, C.C., Bjoertomt, O., Schenkluhn, B., Bestmann, S., Blankenburg, F., Driver, J., and Chambers, C.D. (2011). Concurrent TMS-fMRI reveals dynamic interhemispheric influences of the right parietal cortex during exogenously cued visuospatial attention. Eur J Neurosci 33, 991-1000.
33. Herwig, U., Satrapi, P., and Schonfeldt-Lecuona, C. (2003). Using the international 10-20 EEG system for positioning of transcranial magnetic stimulation. Brain Topogr 16, 95-99.
34. Hillis, A.E. (2006). Neurobiology of unilateral spatial neglect. Neuroscientist 12, 153-163.
35. Husain, M., and Kennard, C. (1996). Visual neglect associated with frontal lobe infarction. J Neurol 243, 652-657.
36. Jewell, G., and Mccourt, M.E. (2000). Pseudoneglect: a review and meta-analysis of performance factors in line bisection tasks. Neuropsychologia 38, 93-110.
37. Karnath, H.O., Fruhmann Berger, M., Kuker, W., and Rorden, C. (2004). The anatomy of spatial neglect based on voxelwise statistical analysis: a study of 140 patients. Cereb Cortex 14, 1164-1172.
38. Kincade, J.M., Abrams, R.A., Astafiev, S.V., Shulman, G.L., and Corbetta, M. (2005). An event- related functional magnetic resonance imaging study of voluntary and stimulus-driven orienting of attention. J Neurosci 25, 4593-4604.
39. Kinsbourne, M. (1977). Hemi-neglect and hemisphere rivalry, in Hemi-Inattention and Hemisphere Specialization, eds. E.A. Weinstein & R.P. Friedland. (New York, U.S.A.: Raven Press), 41-49.
40. Leibovitch, F.S., Black, S.E., Caldwell, C.B., Ebert, P.L., Ehrlich, L.E., and Szalai, J.P. (1998). Brain-behavior correlations in hemispatial neglect using CT and SPECT: the Sunnybrook Stroke Study. Neurology 50, 901-908.
41. Li, X., Ricci, R., Large, C.H., Anderson, B., Nahas, Z., Bohning, D.E., and George, M.S. (2010).Interleaved transcranial magnetic stimulation and fMRI suggests that lamotrigine and valproic acid have different effects on corticolimbic activity. Psychopharmacology (Berl) 209, 233-244.
42. Maguire, A.M., and Ogden, J.A. (2002). MRI brain scan analyses and neuropsychological profiles of nine patients with persisting unilateral neglect. Neuropsychologia 40, 879-887.
43. Marshall, J.C., Fink, G.R., Halligan, P.W., and Vallar, G. (2002). Spatial awareness: a function of the posterior parietal lobe? Cortex 38, 253-257; discussion 258-260.
44. Medina, J., Kannan, V., Pawlak, M.A., Kleinman, J.T., Newhart, M., Davis, C., Heidler-Gary, J.E., Herskovits, E.H., and Hillis, A.E. (2009). Neural substrates of visuospatial processing in distinct reference frames: evidence from unilateral spatial neglect. J Cogn Neurosci 21, 2073-2084.
45. Mesulam, M.M. (1999). Spatial attention and neglect: parietal, frontal and cingulate contributions to the mental representation and attentional targeting of salient extrapersonal events. Philos Trans R Soc LondB Biol Sci 354, 1325-1346.
46. Milner, A.D., Harvey, M., Roberts, R.C., and Forster, S.V. (1993). Line bisection errors in visual neglect: misguided action or size distortion? Neuropsychologia 31, 39-49.
47. Moliadze, V., Zhao, Y., Eysel, U., and Funke, K. (2003). Effect of transcranial magnetic stimulation on single-unit activity in the cat primary visual cortex. J Physiol 553, 665-679.
48. Mort, D.J., Malhotra, P., Mannan, S.K., Rorden, C., Pambakian, A., Kennard, C., and Husain, M. (2003). The anatomy of visual neglect. Brain 126, 1986-1997.
49. Nowak, D.A., Grefkes, C., Dafotakis, M., Eickhoff, S., Kust, J., Karbe, H., and Fink, G.R. (2008). Effects of low-frequency repetitive transcranial magnetic stimulation of the contralesional primary motor cortex on movement kinematics and neural activity in subcortical stroke. Arch Neurol 65, 741-747.
50. Pascual-Leone, A., Walsh, V., and Rothwell, J. (2000). Transcranial magnetic stimulation in cognitive neuroscience--virtual lesion, chronometry, and functional connectivity. Curr Opin Neurobiol 10, 232-237.
51. Rafal, R. (2001). Virtual neurology. Nat Neurosci 4, 862-864.
52. Ricci, R., and Chatterjee, A. (2004). Sensory and response contributions to visual awareness in extinction. Experimental Brain Research 157, 85-93.
53. Rorden, C., Karnath, H.O., and Bonilha, L. (2007). Improving lesion-symptom mapping. J Cogn Neurosci 19, 1081-1088.
54. Ruff, C.C., Bestmann, S., Blankenburg, F., Bjoertomt, O., Josephs, O., Weiskopf, N., Deichmann, R., and Driver, J. (2008). Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb Cortex 18, 817-827.
55. Ruff, C.C., Blankenburg, F., Bjoertomt, O., Bestmann, S., Freeman, E., Haynes, J.D., Rees, G., Josephs, O., Deichmann, R., and Driver, J. (2006). Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol 16, 1479-1488.
56. Ruff, C.C., Blankenburg, F., Bjoertomt, O., Bestmann, S., Weiskopf, N., and Driver, J. (2009a). Hemispheric differences in frontal and parietal influences on human occipital cortex: direct confirmation with concurrent TMS-fMRI. J Cogn Neurosci 21, 1146-1161.
57. Ruff, C.C., Driver, J., and Bestmann, S. (2009b). Combining TMS and fMRI: from 'virtual lesions' to functional-network accounts of cognition. Cortex 45, 1043-1049.