Diffusion tensor fiber tracking shows distinct corticostriatal circuits in humans
Abstract
A landmark of corticostriatal connectivity in nonhuman primates is that cortical connections are organized into a set of discrete circuits. Each circuit is assumed to perform distinct behavioral functions. In animals, most connectivity studies are performed using invasive tracing methods, which are nonapplicable in humans. To test the proposal that corticostriatal connections are organized as multiple circuits in humans, we used diffusion tensor imaging axonal tracking, a new magnetic resonance technique that allows demonstration of fiber tracts in a noninvasive manner. Diffusion tensor imaging–based fiber tracking showed that the posterior (sensorimotor), anterior (associative), and ventral (limbic) compartments of the human striatum have specific connections with the cortex, and particularly the frontal lobes. These results provide the first direct demonstration of distinct corticostriatal connections in humans.
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Structural connectivity imaging techniques in humans have begun to find support for the general organization of the corticostriatal circuitry described.
“The majority of these connectivity studies utilize neuroanatomical tracing in non-human species, but structural connectivity imaging techniques in humans have begun to find support for the general organization of the corticostriatal circuitry described here 9.”
From The social brain and reward: Social information processing in the human striatum (2014) · cites this paper as [9]
Cites
Parallel organization of functionally segregated circuits linking basal ganglia and cortex
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002041 · Cited by 8,527 · see citing works
Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging
Mori, S., Crain, B. J., Chacko, V. P., & van Zijl, P. C. M. (1999) · Annals of Neurology · doi:10.1002/1531-8249(199902)45:2 · Cited by 3,479 · see citing works
Basal ganglia and cerebellar loops: motor and cognitive circuits
Middleton, F. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(99)00040-5 · Cited by 1,940 · see citing works
FMRI visualization of brain activity during a monetary incentive delay task
Knutson, B., Westdorp, A., Kaiser, E., & Hommer, D. (2000) · NeuroImage · doi:10.1006/nimg.2000.0593 · Cited by 1,414 · see citing works
Functional imaging of neural responses to expectancy and experience of monetary gains and losses
Breiter, H. C., Aharon, I., Kahneman, D., Dale, A., & Shizgal, P. (2001) · Neuron · doi:10.1016/s0896-6273(01)00303-8 · Cited by 1,404 · see citing works
Multiple reward signals in the brain
Schultz, W. (2000) · Nature Reviews Neuroscience · doi:10.1038/35044563 · Cited by 1,303 · see citing works
Alheid, G. F., & Heimer, L. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90217-5 · Cited by 1,217 · see citing works
Cavada, C., & Goldman, P. S. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902870403 · Cited by 1,127 · see citing works
Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey
Selemon, L. D., & Goldman-Rakic, P. S. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-03-00776.1985 · Cited by 1,074 · see citing works
Cortical areas and the selection of movement: a study with positron emission tomography
Deiber, M., Passingham, R. E., Colebatch, J. G., Friston, K. J., Nixon, P. D., & Frackowiak, R. S. J. (1991) · Experimental Brain Research · doi:10.1007/bf00231461 · Cited by 895 · see citing works
Künzle, H. (1975) · Brain Research · doi:10.1016/0006-8993(75)90384-4 · Cited by 714 · see citing works
Neural systems engaged by planning: A PET study of the Tower of London task
Baker, S. C., Rogers, R. D., Owen, A. M., Frith, C. D., Dolan, R. J., Frackowiak, R. S. J., & Robbins, T. W. (1996) · Neuropsychologia · doi:10.1016/0028-3932(95)00133-6 · Cited by 635 · see citing works
The orbital and medial prefrontal circuit through the primate basal ganglia
Haber, S., Kunishio, K., Mizobuchi, M., & Lynd-Balta, E. (1995) · The Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04851.1995 · Cited by 605 · see citing works
Imaging cortical association tracts in the human brain using diffusion‐tensor‐based axonal tracking
Mori, S., Kaufmann, W. E., Davatzikos, C. A., Stieltjes, B., Amodei, L., Fredericksen, K., Pearlson, G. D., Melhem, E. R., Solaiyappan, M., Raymond, G. V., et al. (2002) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10074 · Cited by 558 · see citing works
Diffusion Tensor Imaging and Axonal Tracking in the Human Brainstem
Stieltjes, B., Kaufmann, W. E., van Zijl, P. C. M., Fredericksen, K., Pearlson, G. D., Solaiyappan, M., & Mori, S. (2001) · NeuroImage · doi:10.1006/nimg.2001.0861 · Cited by 492 · see citing works
Anatomy of Motor Learning. II. Subcortical Structures and Learning by Trial and Error
Jueptner, M., Frith, C., Brooks, D. J., Frackowiak, R. S. J., & Passingham, R. E. (1997) · Journal of Neurophysiology · doi:10.1152/jn.1997.77.3.1325 · Cited by 466 · see citing works
Regularization of Diffusion-Based Direction Maps for the Tracking of Brain White Matter Fascicles
Poupon, C., Clark, C., Frouin, V., Régis, J. M., Isabelle Bloch, A., Bihan, D. L., & Mangin, J. (2000) · NeuroImage · doi:10.1006/nimg.2000.0607 · Cited by 426 · see citing works
Self-citationThe amygdalostriatal projections in the monkey. An anterograde tracing study
Russchen, F. T., Bakst, I., Amaral, D. G., & Price, J. L. (1985) · Brain Research · doi:10.1016/0006-8993(85)90530-x · Cited by 395 · cited 2× · see citing works
“As in this study, amygdala afferents to the ventral striatum courses through the substantia innominata and the nucleus basalis of Meynert.(26) Except for the anterior cingulate cortex, these data are in agreement with our results.”
ResultPrefrontostriatal connections in relation to cortical architectonic organization in rhesus monkeys
Yeterian, E. H., & Pandya, D. N. (1991) · Journal of Comparative Neurology · doi:10.1002/cne.903120105 · Cited by 351 · see citing works
Flaherty, A. W., & Graybiel, A. M. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-03-01120.1993 · Cited by 338 · see citing works
Primate cingulostriatal projection: Limbic striatal versus sensorimotor striatal input
Kunishio, K., & Haber, S. N. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903500302 · Cited by 290 · see citing works
Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque
Hedreen, J. C., & Delong, M. R. (1991) · The Journal of Comparative Neurology · doi:10.1002/cne.903040406 · Cited by 245 · see citing works
Friedman, D. P., Aggleton, J. P., & Saunders, R. C. (2002) · The Journal of Comparative Neurology · doi:10.1002/cne.10336 · Cited by 245 · see citing works
Inase, M., Tokuno, H., Nambu, A., Akazawa, T., & Takada, M. (1999) · Brain Research · doi:10.1016/s0006-8993(99)01531-0 · Cited by 227 · see citing works
Amygdaloid projections to ventromedial striatal subterritories in the primate
Fudge, J. L., Kunishio, K., Walsh, P., Richard, C., & Haber, S. N. (2002) · Neuroscience · doi:10.1016/s0306-4522(01)00546-2 · Cited by 226 · see citing works
Lavoie, B. A., Smith, Y., & Parent, A. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902890104 · Cited by 203 · see citing works
Distortion correction and robust tensor estimation for MR diffusion imaging
Mangin, J., Poupon, C., Clark, C., Bihan, D. L., & Isabelle Bloch, A. (2002) · Medical Image Analysis · doi:10.1016/s1361-8415(02)00079-8 · Cited by 195 · see citing works
Self-citationA neural network model of neural activity in the monkey globus pallidus
Brotchie, P., Iansek, R., & Horne, M. K. (1991) · Neuroscience Letters · doi:10.1016/0304-3940(91)90330-v · Cited by 55 · see citing works
Lehéricy, S., de Moortele, P. V., Löbel, E., Paradis, A., Vidailhet, M., Frouin, V., Neveu, P., Agid, Y., Marsault, C., & Bihan, D. L. (1998) · Annals of Neurology · doi:10.1002/ana.410440319 · Cited by 54 · see citing works
Self-citationGlover (2000) · doi:10.1002/1522-2594(200007)44:1
Yeterian (1998) · doi:10.1002/(sici)1096-9861(19980928)399:3
Basser (2000) · doi:10.1002/1522-2594(200010)44:4
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Amodio, D. M., & Frith, C. D. (2006) · Nature Reviews Neuroscience · doi:10.1038/nrn1884 · Cited by 3,782 · see citing works
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Catani, M., Jones, D. K., & ffytche, D. H. (2005) · Annals of Neurology · doi:10.1002/ana.20319 · Cited by 1,832 · see citing works
Aron, A. R. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.07.024 · Cited by 1,236 · see citing works
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del Campo, N., Chamberlain, S. R., Sahakian, B. J., & Robbins, T. W. (2011) · Biological Psychiatry · doi:10.1016/j.biopsych.2011.02.036 · Cited by 685 · see citing works
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Pessiglione, M., Schmidt, L., Draganski, B., Kalisch, R., Lau, H., Dolan, R. J., & Frith, C. D. (2007) · Science · doi:10.1126/science.1140459 · Cited by 634 · see citing works
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Jbabdi, S., & Johansen-Berg, H. (2011) · Brain Connectivity · doi:10.1089/brain.2011.0033 · Cited by 614 · see citing works
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Turken, U., Whitfield-Gabrieli, S., Bammer, R., Baldo, J. V., Dronkers, N. F., & Gabrieli, J. D. E. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.03.057 · Cited by 500 · see citing works
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Foerde, K., Poldrack, R. A., Knowlton, B. J., Sabb, F. W., Bookheimer, S. Y., Bilder, R. M., Guthrie, D., Granholm, E., Nuechterlein, K. H., Marder, S. R., et al. (2008) · Neuropsychology · doi:10.1037/0894-4105.22.1.100 · Cited by 67 · see citing works
Hamzei, F., Glauche, V., Schwarzwald, R., & May, A. (2012) · NeuroImage · doi:10.1016/j.neuroimage.2011.10.089 · Cited by 56 · see citing works
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- Authors
- Lehéricy, S., Ducros, M., Van De Moortele, P., Francois, C., Thivard, L., Poupon, C., Swindale, N., Ugurbil, K., & Kim, D.
- Affiliations
- Boston University (US)
- Corresponding author
- Lehéricy, Stéphane
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2004-03-22
- Volume
- 55
- Issue
- 4
- Pages
- 522-529
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- OpenAlex
- W2172252744
- Cited by
- 542
- References
- 32
- Citations by year
- 2026: 8 · 2025: 7 · 2024: 7 · 2023: 13 · 2022: 11 · 2021: 22 · 2020: 23 · 2019: 32 · 2018: 27 · 2017: 29 · 2016: 33 · 2015: 39 · 2014: 26 · 2013: 43 · 2012: 41
- FWCI
- 16.59
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- NIH (BTRR P41-RR008079)
- Keck Foundation
- Human Frontiers Science Program
- Inciting Joint Actions Committee (AC1-6503H)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- corticostriatal circuits, corticostriatal connectivity, diffusion tensor imaging, tractography, human striatum, sensorimotor striatum, associative striatum, limbic striatum
- MeSH terms
- Adult, Cerebral Cortex, Corpus Striatum, Female, Humans, Male, Nerve Fibers, Nerve Net, Diffusion Magnetic Resonance Imaging
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