The variation of function across the human insula mirrors its patterns of structural connectivity: Evidence from in vivo probabilistic tractography

NeuroImage

Volumn 59, Issue 4, 2012, Pages 3514-3521

  Cloutman, Lauren L ^a   Binney, Richard J ^a   Drakesmith, Mark ^a   Parker, Geoffrey J M ^a   Lambon Ralph, Matthew A ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Diffusion; Dual route; Functional specialization; Neural networks; White matter

Indexed keywords

ADULT; ARTICLE; BEHAVIOR; BRAIN FUNCTION; BRAIN MAPPING; BRAIN REGION; COGNITION; DIFFUSION TENSOR IMAGING; EMOTION; FEMALE; HUMAN; HUMAN EXPERIMENT; IN VIVO STUDY; INSULA; MALE; NERVOUS SYSTEM PARAMETERS; NORMAL HUMAN; PRIORITY JOURNAL; SOUND; SPEECH; STRUCTURAL CONNECTIVITY;

ADULT; BRAIN MAPPING; CEREBRAL CORTEX; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; MALE; MIDDLE AGED; YOUNG ADULT;

EID: 84855168539     PISSN: 10538119     EISSN: 10959572     Source Type: Journal    
DOI: 10.1016/j.neuroimage.2011.11.016     Document Type: Article

References (74)

1. Ackermann H., Riecker A. The contribution of the insula to motor aspects of speech production: a review and a hypothesis. Brain Lang. 2004, 89:320-328.
2. Afif A., Hoffmann D., Becq G., Guenot M., Magnin M., Mertens P. MRI-based definition of a stereotactic two-dimensional template of the human insula. Stereotact. Funct. Neurosurg. 2009, 87:385-394.
3. Alexander G.E., Crutcher M.D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990, 13:266-271.
4. Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage 2007, 38:95-113.
5. Baliki M.N., Geha P.Y., Apkarian A.V. Parsing pain perception between nociceptive representation and magnitude estimation. J. Neurophysiol. 2009, 101:875-887.
6. Bamiou D.-E., Musiek F.E., Luxon L.M. The insula (Island of Reil) and its role in auditory processing. Literature review. Brain Res. Rev. 2003, 42:143-154.
7. Bamiou D.-E., Musiek F.E., Stow I., Stevens J., Cipolotti L., Brown M.M., Luxon L.M. Auditory temporal processing deficits in patients with insular stroke. Neurology 2006, 67:614-619.
8. Beckman M., Johansen-Berg H., Rushworth M.F.S. Connectivity-based parcellation of human cingulate cortex and its relation to functional specialization. J. Neurosci. 2009, 29:1175-1190.
9. Behrens T.E.J., Johansen-Berg H. Relating connectional architecture to grey matter function using diffusion imaging. Philos. Trans. R. Soc. B 2005, 360:903-911.
10. Bengtsson S.L., Ehrsson H., Forssberg H., Ullen F. Dissociating brain regions controlling the temporal and ordinal structure of learned movement sequences. Eur. J. Neurosci. 2004, 19:2591-2602.
11. Berlin P., Zatorre R.J. 'What', 'where' and 'how' in auditory cortex. Nat. Neurosci. 2000, 3:965-966.
12. Caruana F., Jezzini A., Sbriscla-Floretti B., Rizzolatti G., Gallese V. Emotional and social behaviours elicited by electrical stimulation of the insula in the macaque monkey. Curr. Biol. 2011, 21:195-199.
13. Cauda F., D'Agata F., Sacco K., Duca S., Geminiani G., Vercelli A. Functional connectivity of the insula in the resting brain. Neuroimage 2011, 55:8-23.
14. Cerliani, L., Thomas, R.M., Jbabdi, S., Siero, J.C.W., Nanetti, L., Crippa, A., Gazzola, V., D'Arceuil, H., Keysers, C., in press. Probabilistic tractography recovers a rostrocaudal trajectory of connectivity variability in the human insular cortex. Hum. Brain Mapp. (Electronic publication ahead of print).
15. Cohen J.D., Mock J.R., Nichols T., Zadina J., Corey D.M., Lemen L., Bellugi U., Galaburda A., Reiss A., Foundas A.L. Morphometry of human insular cortex and insular volume reduction in Williams syndrome. J. Psychiatr. Res. 2010, 44:81-89.
16. Cohen, J.R., Berkman, E.T., Lieberman, M.D., in press. Intentional and incidental self-control in ventrolateral PFC. In: Stuss, D.T., Knight, R.T., editors. The Oxford Handbook of Frontal Lobe Functions. Oxford: Oxford University Press.
17. Colativa F.B., Weisberg D.H. Spatio-temporal pattern discrimination in cats with insular-temporal lesions. Brain Res. Bull. 1978, 3:7-9.
18. Craig A.D. How do you feel - now? The anterior insula and human awareness. Nat. Rev. Neurosci. 2009, 10:59-70.
19. Damoiseaux J.S., Greicius M.D. Greater than the sum of its parts: a review of studies combining structural connectivity and resting-state functional connectivity. Brain Struct. Funct. 2009, 213:525-533.
20. Deen B., Pitskel N.B., Pelphrey K.A. Three systems of insular functional connectivity identified with cluster analysis. Cereb. Cortex 2011, 21:1498-1506.
21. Deffains M., Legallet E., Apicella P. Modulation of neuronal activity in the monkey putamen associated with changes in the habitual order of sequential movements. J. Neurophysiol. 2010, 104:1355-1359.
22. Descoteaux M., Deriche R., Knosche T.R., Anwander A. Deterministic and probabilistic tractography based on complex fibre orientation distributions. IEEE Trans. Med. Imaging 2009, 28:269-286.
23. Dosenbach N.U.F., Visscher K.M., Palmer E.D., Miezin F.M., Wenger K.K., Kang H.C., Burgund E.D., Grimes A.L., Schlaggar B.L., Petersen S.E. A core system for the implementation of task sets. Neuron 2006, 50:799-812.
24. Dosenbach N.U.F., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A.T., Fox M.D., Snyder A.Z., Vincent J.L., Raichle M.E., Schlaggar B.L., Petersen S.E. Distinct brain networks for adaptive and stable task control in humans. Proc. Natl. Acad. Sci. USA 2007, 104:11073-11078.
25. Dronkers N.F. A new brain region for coordinating speech articulation. Nature 1996, 384:159-161.
26. Eckert M.A., Menon V., Walczak A., Ahlstrom J., Denslow S., Horwitz A., Dubno J.R. At the heart of the ventral attention system: the right anterior insula. Hum. Brain Mapp. 2009, 30:2530-2541.
27. Eickhoff S.B., Heim S., Zilles K., Amunts K. A systems perspective on the effective connectivity of overt speech production. Philos. Trans. R. Soc. A 2009, 376:2399-2421.
28. Embleton K., Haroon H., Morris D., Lambon Ralph M., Parker G. Distortion correction for diffusion weighted MRI tractography and fMRI in the temporal lobes. Hum. Brain Mapp. 2010, 31:1570-1587.
29. Fernandez-Miranda J.C., Rhoton A.L., Alvarez-Linera J., Kakizawa Y., Choi C., de Oliveira E.P. Three-dimensional microsurgical and tractographic anatomy of the white matter of the human brain. Neurosurgery 2008, 62:989-1027.
30. Houde J.F., Jordan M.I. Sensorimotor adaptation in speech production. Science 1998, 279:1213-1216.
31. Jabbi M., Bastiaansen J., Keysers C. A common anterior insula representation of disgust observation, experience and imagination shows divergent functional connectivity pathways. PLoS One 2008, 3:e2939.
32. Jones D.K. Studying connections in the living brain with diffusion MRI. Cortex 2008, 44:936-952.
33. Kalani M.Y.S., Kalani M.A., Gwinn R., Keogh B., Tse V.C.K. Embryological development of the human insula and its implications for the spread and resection of insular gliomas. Neurosurg. Focus 2009, 27:E2.
34. Kier E.L., Staib L.H., Davis L.M., Bronen R.A. MR imaging of the temporal stem: anatomic dissection tractography of the uncinate fasciculus, inferior occipitofrontal fasciculus, and Meyer's loop of the optic radiation. Am. J. Neuroradiol. 2004, 25:677-691.
35. Kurth F., Zilles K., Fox P.T., Laird A.R., Eickhoff S.B. A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct. Funct. 2010, 214:519-534.
36. Levy B.J., Wagner A.D. Cognitive control and right ventrolateral prefrontal cortex: reflexive reorienting, motor inhibition, and action updating. Ann. N. Y. Acad. Sci. 2011, 1224:40-62.
37. Makris N., Kennedy D.N., McInerney S., Sorensen A.G., Wang R., Caviness V.S., Pandya D.N. Segmentation of subcomponents within the superior longitudinal fascicle in humans: a quantitative, in vivo, DT-MRI study. Cereb. Cortex 2005, 15:854-869.
38. Maldjian J.A., Laurienti P.J., Burdette J.B., Kraft R.A. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage 2003, 19:1233-1239.
39. Martino J., Brogna C., Robles S.G., Vergani F., Duffau H. Anatomic dissection of the inferior fronto-occipital fasciculus revisited in the lights of brain stimulation data. Cortex 2010, 46:691-699.
40. Medford N., Critchley H.D. Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct. Funct. 2010, 214:535-549.
41. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Struct. Funct. 2010, 214:655-667.
42. Mesulam M.M., Mufson E.J. Insula of the old world monkey. I: architectonics in the insulo-orbito-temporal component of the paralimbic brain. J. Comp. Neurol. 1982, 212:1-22.
43. Mesulam M.M., Mufson E.J. Insula of the old world monkey. III: efferent cortical output and comments on function. J. Comp. Neurol. 1982, 212:38-52.
44. Mishkin M., Ungerleider L.G., Macko K.A. Object vision and spatial vision: two cortical pathways. Trends Neurosci. 1983, 6:414-417.
45. Morris D.M., Embleton K.V., Parker G.J.M. Probabilistic fibre tracking: differentiation of connections from chance events. Neuroimage 2008, 42:1329-1339.
46. Mufson E.J., Mesulam M.M. Insula of the old world monkey. II: afferent cortical input and comments on the claustrum. J. Comp. Neurol. 1982, 212:23-37.
47. Mutschler I., Wieckhorst B., Kowalevski S., Derix J., Wentlandt J., Schulze-Bonhage A., Ball T. Functional organisation of the human anterior insular cortex. Neurosci. Lett. 2009, 457:66-70.
48. Naidich T.P., Kang E., Fatterpekar G.M., Delman B.N., Gultekin S.H., Wolfe D., Ortiz O., Yousry I., Weismann M., Yousry T.A. The insula: anatomic study and MR imaging display at 1.5T. Am. J. Neuroradiol. 2004, 25:222-232.
49. O'Reilly R.C. The what and how of prefrontal cortical organisation. Trends Neurosci. 2010, 33:355-361.
50. Oldfield R.C. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia 1971, 9:97-113.
51. Parker G.J.M., Alexander D.C. Probabilistic Monte Carlo based mapping of cerebral connections utilising whole-brain crossing fibre information. Inf. Process. Med. Imaging 2003, 18:684-695.
52. Parker G.J.M., Alexander D.C. Probabilistic anatomical connectivity derived from the microscopic persistence angular structure of cerebral tissue. Philos. Trans. R. Soc. B 2005, 360:893-902.
53. Parker G.J.M., Haroon H.A., Wheeler-Kingshott C.A.M. A framework for a streamline-based probabilistic index of connectivity PICo using a structural interpretation of MRI diffusion measurements. J. Magn. Reson. Imaging 2003, 18:242-254.
54. Parker G.J.M., Luzzi S., Alexander D.C., Wheeler-Kingshott C.A.M., Ciccarelli O., Lambon Ralph M.A. Lateralization of ventral and dorsal auditory-anguage pathways in the human brain. Neuroimage 2005, 24:656-666.
55. Plaut D.C. Graded modality-specific specialisation in semantics: a computational account of optic aphasia. Cogn. Neuropsychol. 2002, 19:603-639.
56. Price C.J. The anatomy of language: a review of 100 fMRI studies published in 2009. Ann. N. Y. Acad. Sci. 2010, 1191:62-88.
57. Riecker A., Ackermann H., Wildgruber D., Dogil G., Grodd W. Opposite hemispheric lateralisation effects during speaking and singing at motor cortex, insula and cerebellum. Neuroreport 2000, 11:1997-2000.
58. Schmahmann J.D., Pandya D.N., Wang R., Dai G., D'Arceuil H.E., de Crespigny A.J., Wedeen V.J. Association fibre pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007, 130:630-653.
59. Scott S.K., Blank C.C., Rosen S., Wise R.J.S. Identification of a pathway for intelligible speech in the left temporal lobe. Brain 2000, 123:2400-2406.
60. Seeley W.W., Menon V., Schatzberg A.F., Keller J., Glover G.H., Kenna H., Reiss A.L., Greicius M.D. Dissociable intrinsic connectivity networks for salience processing and executive control. J. Neurosci. 2007, 27:2349-2356.
61. Small D.M. Taste representation in the human insula. Brain Struct. Funct. 2010, 214:551-561.
62. Tanriover N., Rhoton A.L., Kawashima M., Ulm A.J., Yasuda A. Microsurgical anatomy of the insula and the sylvaina fissure. J. Neurosurg. 2004, 100:891-922.
63. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Hum. Brain Mapp. 2009, 30:2731-2745.
64. Tournier J.-D., Yeh C.-H., Calamante F., Cho K.-H., Connelly A., Lin C.-P. Resolving crossing fibers using constrained spherical deconvolution: validation using diffusion-weighted imaging phantom data. Neuroimage 2008, 42:617-625.
65. Ture U., Yasarcil D.C.H., Al-Mefty O., Yasargil M.G. Topographic anatomy of the insular region. J. Neurosurg. 1999, 90:720-733.
66. Tzourio-Mazoyer N., Landeau B., Papathanassiou D., Crivello F., Etard O., Delcroix N., Mazoyer B., Joliot M. Automated anatomical labelling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 2002, 15:273-289.
67. Uddin L.Q., Mooshagian E., Zaidel E., Scheres A., Margulies D.S., Kelly A.M.C., Shehzad Z., Adelstein J.S., Castellanos F.X., Biswal B.B., Milham M.P. Residual functional connectivity in the split-brain revealed with resting-state functional MRI. Neuroreport 2008, 19:703-709.
68. Umarova R.M., Saur D., Schnell S., Kaller C.P., Vry M.-S., Glauche V., Rijntjes M., Hennig J., Kiselev V., Weiller C. Structural connectivity for visuospatial attention: significance of ventral pathways. Cereb. Cortex 2010, 20:121-129.
69. van den Heuvel M.P., Mandl R.C.W., Kahn R.S., Hulshoff Pol H.E. Functionally linked resting-state networks reflect the underlying structural connectivity architecture of the human brain. Hum. Brain Mapp. 2009, 30:3127-3141.
70. Weich K., Lin C.-S., Brodersen K.H., Bingel U., Ploner M., Tracey I. Anterior insula integrates information about salience into perceptual decisions about pain. J. Neurosci. 2010, 30:16324-16331.
71. Weiller C., Bormann T., Saur D., Musso M., Rijntjes M. How the ventral pathway got lost - and what its recovery might mean. Brain Lang. 2011, 118:29-39.
72. Wise R.J.S., Greene J., Buchel C., Scott S.K. Brain regions involved in articulation. Lancet 1999, 353:1057-1061.
73. Wise R.J.S., Scott S.K., Blank S.C., Mummery C.J., Murphy K., Warburton E.A. Separate neural subsystems within 'Wernicke's area'. Brain 2001, 124:83-95.
74. Zhang D., Snyder A.Z., Shimony J.S., Fox M.D., Raichle M.E. Noninvasive functional and structural connectivity mapping of the human thalamocortical system. Cereb. Cortex 2010, 20:1187-1194.