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Fronto-striatal organization: Defining functionaland microstructural substrates of behaviouralflexibility
Laurel S. Morris a,b, Prantik Kundu c,d, Nicholas Dowell e,Daisy J. Mechelmans c, Pauline Favre f, Michael A. Irvine c,Trevor W. Robbins a,b, Nathaniel Daw g, Edward T. Bullmore b,c,h,i,Neil A. Harrison e and Valerie Voon b,c,h,i,*
a Department of Psychology, University of Cambridge, Cambridge, United Kingdomb Behavioural and Clinical Neuroscience Institute, University of Cambridge, Cambridge, United Kingdomc Department of Psychiatry, University of Cambridge, Addenbrooke's Hospital, Cambridge, United Kingdomd Section on Functional Imaging Methods, National Institute of Mental Health, Bethesda, MD, USAe Department of Psychiatry, Brighton and Sussex Medical School, Brighton, United Kingdomf Laboratory of Psychology and Neurocognition, University Grenoble Alpes, Grenoble, Franceg Center for Neural Science and Department of Psychology, New York University, New York, NY, USAh Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, United Kingdomi NIHR Cambridge Biomedical Research Centre, Cambridge, United Kingdom
a r t i c l e i n f o
Article history:
Received 1 May 2015
Reviewed 14 July 2015
Revised 17 August 2015
Accepted 5 November 2015
Action editor Gui Xue
Published online 18 November 2015
Keywords:
Fronto-striatal loops
Goal-directed
Habit
Microstructure
Neurite density
* Corresponding author. Department of PsyCambridge CB2 0QQ, United Kingdom.
Table 2 e Neural connectivity correlates of learning errors for reward and loss. Whole brain connectivity maps for seedregions of interest (ROI) were correlated with reversal errors for reward and loss separately. Abbreviations: PFC, prefrontalcortex; OFC, orbitofrontal cortex; dlPFC, dorsolateral prefrontal cortex; Z, Z-score statistic following cluster extentthresholding.
Cognition, Eli Lilly, GSK, Merck, Sharpe andDohme, Lundbeck,
Teva and Shire Pharmaceuticals. He is or has been in receipt of
research grants from Lundbeck, Eli Lilly and GSK and is an
editor for Springer-Verlag (Psychopharmacology). The
remaining authors declare no competing financial interests.
The study was funded by the Wellcome Trust Fellowship
grant for VV (093705/Z/10/Z) and Cambridge NIHR Biomedical
Research Centre.
Supplementary material
Supplementary material related to this article can be found at
http://dx.doi.org/10.1016/j.cortex.2015.11.004.
r e f e r e n c e s
Alexander, G. E., & Crutcher, M. D. (1990). Functional architectureof basal ganglia circuits: neural substrates of parallelprocessing. Trends in Neurosciences, 13(7), 266e271.
Alexander, G. E., DeLong, M. R., & Strick, P. L. (1986). Parallelorganization of functionally segregated circuits linking basalganglia and cortex. Annual Review of Neuroscience, 9, 357e381.http://dx.doi.org/10.1146/annurev.ne.09.030186.002041.
Balleine, B. W., & O'Doherty, J. P. (2010). Human and rodenthomologies in action control: corticostriatal determinants ofgoal-directed and habitual action [Research Support, N.I.H.,Extramural Review] Neuropsychopharmacology, 35(1), 48e69.http://dx.doi.org/10.1038/npp.2009.131.
Behrens, T. E., Johansen-Berg, H., Woolrich, M. W., Smith, S. M.,Wheeler-Kingshott, C. A., Boulby, P. A., et al. (2003). Non-invasive mapping of connections between human thalamusand cortex using diffusion imaging. Nature Neuroscience, 6(7),750e757. http://dx.doi.org/10.1038/nn1075.
Block, A. E., Dhanji, H., Thompson-Tardif, S. F., & Floresco, S. B.(2007). Thalamic-prefrontal cortical-ventral striatal circuitrymediates dissociable components of strategy set shifting.Cerebral Cortex, 17(7), 1625e1636. http://dx.doi.org/10.1093/cercor/bhl073.
Chen, L. L., & Wise, S. P. (1995). Supplementary eye fieldcontrasted with the frontal eye field during acquisition ofconditional oculomotor associations. Journal ofNeurophysiology, 73(3), 1122e1134.
Choi, E. Y., Yeo, B. T., & Buckner, R. L. (2012). The organization ofthe human striatum estimated by intrinsic functionalconnectivity [Research Support, N.I.H., Extramural ResearchSupport, Non-U.S. Gov't] Journal of Neurophysiology, 108(8),2242e2263. http://dx.doi.org/10.1152/jn.00270.2012.
Collins, P., Wilkinson, L. S., Everitt, B. J., Robbins, T. W., &Roberts, A. C. (2000). The effect of dopamine depletion fromthe caudate nucleus of the common marmoset (Callithrixjacchus) on tests of prefrontal cognitive function. BehavioralNeuroscience, 114(1), 3e17.
Corbit, L. H., Muir, J. L., & Balleine, B. W. (2001). The role of thenucleus accumbens in instrumental conditioning: evidence ofa functional dissociation between accumbens core and shell.Journal of Neuroscience, 21(9), 3251e3260.
Cox, S. R., Ferguson, K. J., Royle, N. A., Shenkin, S. D.,MacPherson, S. E., MacLullich, A. M., et al. (2014). A systematicreview of brain frontal lobe parcellation techniques inmagnetic resonance imaging. Brain Structure & Function, 219(1),1e22. http://dx.doi.org/10.1007/s00429-013-0527-5.
Daw, N. D., Gershman, S. J., Seymour, B., Dayan, P., & Dolan, R. J.(2011). Model-based influences on humans' choices and
Dayan, P., & Niv, Y. (2008). Reinforcement learning: the good, thebad and the ugly. Current Opinion in Neurobiology, 18(2),185e196. http://dx.doi.org/10.1016/j.conb.2008.08.003.
Desikan, R. S., Segonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C.,Blacker, D., et al. (2006). An automated labeling system forsubdividing the human cerebral cortex on MRI scans into gyralbased regions of interest. NeuroImage, 31(3), 968e980. http://dx.doi.org/10.1016/j.neuroimage.2006.01.021.
Di Martino, A., Scheres, A., Margulies, D. S., Kelly, A. M.,Uddin, L. Q., Shehzad, Z., et al. (2008). Functional connectivityof human striatum: a resting state FMRI study [ResearchSupport, Non-U.S. Gov't] Cerebral Cortex, 18(12), 2735e2747.http://dx.doi.org/10.1093/cercor/bhn041.
Dias, R., Robbins, T. W., & Roberts, A. C. (1996). Dissociation inprefrontal cortex of affective and attentional shifts. Nature,380(6569), 69e72. http://dx.doi.org/10.1038/380069a0.
Dickinson, A. (1985). Actions and habits e the development ofbehavioral autonomy. Philosophical Transactions of the RoyalSociety of London Series B-Biological Sciences, 308(1135), 67e78.http://dx.doi.org/10.1098/Rstb.1985.0010.
Downes, J. J., Roberts, A. C., Sahakian, B. J., Evenden, J. L.,Morris, R. G., & Robbins, T. W. (1989). Impaired extra-dimensional shift performance inmedicated and unmedicatedParkinson's disease: evidence for a specific attentionaldysfunction. Neuropsychologia, 27(11e12), 1329e1343.
Elliott, R., Friston, K. J., & Dolan, R. J. (2000). Dissociable neuralresponses in human reward systems [Research Support, Non-U.S. Gov't] Journal of Neuroscience, 20(16), 6159e6165.
Everitt, B. J., & Robbins, T. W. (2005). Neural systems ofreinforcement for drug addiction: from actions to habits tocompulsion. Nature Neuroscience, 8(11), 1481e1489. http://dx.doi.org/10.1038/nn1579.
Floresco, S. B., Ghods-Sharifi, S., Vexelman, C., & Magyar, O.(2006). Dissociable roles for the nucleus accumbens core andshell in regulating set shifting. Journal of Neuroscience, 26(9),2449e2457. http://dx.doi.org/10.1523/JNEUROSCI.4431-05.2006.
Gillan, C. M., Papmeyer, M., Morein-Zamir, S., Sahakian, B. J.,Fineberg, N. A., Robbins, T. W., et al. (2011). Disruption in thebalance between goal-directed behavior and habit learning inobsessive-compulsive disorder. American Journal of Psychiatry,168(7), 718e726. http://dx.doi.org/10.1176/Appi.Ajp.2011.10071062.
Glascher, J., Daw, N., Dayan, P., & O'Doherty, J. P. (2010). Statesversus rewards: dissociable neural prediction error signalsunderlying model-based and model-free reinforcementlearning. Neuron, 66(4), 585e595. http://dx.doi.org/10.1016/J.Neuron.2010.04.016.
Glascher, J., Hampton, A. N., & O'Doherty, J. P. (2009). Determininga role for ventromedial prefrontal cortex in encoding action-based value signals during reward-related decision making.Cerebral Cortex, 19(2), 483e495. http://dx.doi.org/10.1093/cercor/bhn098.
Groenewegen, H. J., Wright, C. I., Beijer, A. V. J., & Voorn, P. (1999).Convergence and segregation of ventral striatal inputs andoutputs. Advancing from the Ventral Striatum to the ExtendedAmygdala, 877, 49e63. http://dx.doi.org/10.1111/J.1749-6632.1999.Tb09260.X.
Groman, S. M., James, A. S., Seu, E., Crawford, M. A.,Harpster, S. N., & Jentsch, J. D. (2013). Monoamine levelswithin the orbitofrontal cortex and putamen interact topredict reversal learning performance [Research Support,N.I.H., Extramural] Biological Psychiatry, 73(8), 756e762. http://dx.doi.org/10.1016/j.biopsych.2012.12.002.
Haber, S. N. (2003). The primate basal ganglia: parallel andintegrative networks. Journal of Chemical Neuroanatomy, 26(4),317e330. http://dx.doi.org/10.1016/J.Jchemneu.2003.10.003.
Haber, S. N., & Knutson, B. (2010). The reward circuit: linkingprimate anatomy and human imaging.Neuropsychopharmacology, 35(1), 4e26. http://dx.doi.org/10.1038/npp.2009.129.
Hampshire, A., Chaudhry, A. M., Owen, A. M., & Roberts, A. C.(2012). Dissociable roles for lateral orbitofrontal cortex andlateral prefrontal cortex during preference driven reversallearning. NeuroImage, 59(4), 4102e4112. http://dx.doi.org/10.1016/j.neuroimage.2011.10.072.
Jacobs, B., Schall, M., Prather, M., Kapler, E., Driscoll, L., Baca, S.,et al. (2001). Regional dendritic and spine variation in humancerebral cortex: a quantitative Golgi study. Cerebral Cortex,11(6), 558e571. http://dx.doi.org/10.1093/Cercor/11.6.558.
Jespersen, S. N., Bjarkam, C. R., Nyengaard, J. R.,Chakravarty, M. M., Hansen, B., Vosegaard, T., et al. (2010).Neurite density from magnetic resonance diffusionmeasurements at ultrahigh field: comparison withlight microscopy and electron microscopy. NeuroImage,49(1), 205e216. http://dx.doi.org/10.1016/j.neuroimage.2009.08.053.
Jespersen, S. N., Leigland, L. A., Cornea, A., & Kroenke, C. D. (2012).Determination of axonal and dendritic orientationdistributions within the developing cerebral cortex bydiffusion tensor imaging. IEEE Transactions on Medical Imaging,31(1), 16e32. http://dx.doi.org/10.1109/TMI.2011.2162099.
Jung, W. H., Jang, J. H., Park, J. W., Kim, E., Goo, E. H., Im, O. S.,et al. (2014). Unravelling the intrinsic functional organizationof the human striatum: a parcellation and connectivity studybased on resting-state FMRI. PLoS One, 9(9), e106768. http://dx.doi.org/10.1371/journal.pone.0106768.
Kaden, E., Knosche, T. R., & Anwander, A. (2007). Parametricspherical deconvolution: Inferring anatomical connectivityusing diffusion MR imaging. NeuroImage, 37(2), 474e488. http://dx.doi.org/10.1016/J.Neuroimage.2007.05.012.
Klanker, M., Post, G., Joosten, R., Feenstra, M., & Denys, D. (2013).Deep brain stimulation in the lateral orbitofrontal corteximpairs spatial reversal learning. Behavioural Brain Research,245, 7e12. http://dx.doi.org/10.1016/j.bbr.2013.01.043.
Kreitzer, A. C., & Malenka, R. C. (2008). Striatal plasticity and basalganglia circuit function. Neuron, 60(4), 543e554. http://dx.doi.org/10.1016/J.Neuron.2008.11.005.
Kringelbach, M. L., & Rolls, E. T. (2003). Neural correlates of rapidreversal learning in a simple model of human socialinteraction [Clinical Trial Research Support, Non-U.S. Gov't]NeuroImage, 20(2), 1371e1383. http://dx.doi.org/10.1016/S1053-8119(03)00393-8.
Kuhnen, C. M., & Knutson, B. (2005). The neural basis of financialrisk taking. Neuron, 47(5), 763e770. http://dx.doi.org/10.1016/j.neuron.2005.08.008.
Kundu, P., Brenowitz, N. D., Voon, V., Worbe, Y., Vertes, P. E.,Inati, S. J., et al. (2013). Integrated strategy for improvingfunctional connectivity mapping using multiecho fMRI.Proceedings of the National Academy of Sciences of the United Statesof America, 110(40), 16187e16192. http://dx.doi.org/10.1073/Pnas.1301725110.
Kundu, P., Inati, S. J., Evans, J. W., Luh, W. M., & Bandettini, P. A.(2012). Differentiating BOLD and non-BOLD signals in fMRItime series using multi-echo EPI. NeuroImage, 60(3), 1759e1770.http://dx.doi.org/10.1016/j.neuroimage.2011.12.028.
Lucantonio, F., Stalnaker, T. A., Shaham, Y., Niv, Y., &Schoenbaum, G. (2012). The impact of orbitofrontaldysfunction on cocaine addiction [Research Support, N.I.H.,Extramural Review] Nature Neuroscience, 15(3), 358e366. http://dx.doi.org/10.1038/nn.3014.
Manes, F., Sahakian, B., Clark, L., Rogers, R., Antoun, N.,Aitken, M., et al. (2002). Decision-making processesfollowing damage to the prefrontal cortex. Brain, 125(Pt 3),624e639.
Mardia, K. V., & Jupp, P. E. (1990). Directional statistics. John Wiley &Sons, Ltd. Wiley series in probability and statistics.
Middleton, F. A., & Strick, P. L. (2000). Basal ganglia and cerebellarloops: motor and cognitive circuits. Brain Research. BrainResearch Reviews, 31(2e3), 236e250.
Morris, J. S., & Dolan, R. J. (2001). Involvement of human amygdalaand orbitofrontal cortex in hunger-enhanced memory for foodstimuli. Journal of Neuroscience, 21(14), 5304e5310.
Morris, L. S., Kundu, P., Baek, K., Irvine, M. A., Mechelmans, D. J.,Wood, J., et al. (2015). Jumping the gun: mapping neuralcorrelates of waiting impulsivity and relevance across alcoholmisuse. Biological Psychiatry. http://dx.doi.org/10.1016/j.biopsych.2015.06.009.
Nachev, P., Kennard, C., & Husain, M. (2008). Functional role of thesupplementary and pre-supplementary motor areas. NatureReviews Neuroscience, 9(11), 856e869. http://dx.doi.org/10.1038/nrn2478.
O'doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., &Andrews, C. (2001). Abstract reward and punishmentrepresentations in the human orbitofrontal cortex. NatureNeuroscience, 4(1), 95e102.
Ongur, D., Ferry, A. T., & Price, J. L. (2003). Architectonicsubdivision of the human orbital andmedial prefrontal cortex.Journal of Comparative Neurology, 460(3), 425e449. http://dx.doi.org/10.1002/cne.10609.
Ongur, D., & Price, J. L. (2000). The organization of networkswithin the orbital and medial prefrontal cortex of rats,monkeys and humans. Cerebral Cortex, 10(3), 206e219.
Panagiotaki, E., Schneider, T., Siow, B., Hall, M. G., Lythgoe, M. F.,& Alexander, D. C. (2012). Compartment models of thediffusion MR signal in brain white matter: a taxonomy andcomparison. NeuroImage, 59(3), 2241e2254. http://dx.doi.org/10.1016/j.neuroimage.2011.09.081.
Parent, A., & Hazrati, L. N. (1995). Functional anatomy of the basalganglia. I. The cortico-basal ganglia-thalamo-cortical loop.Brain Research. Brain Research Reviews, 20(1), 91e127.
Pessiglione, M., Seymour, B., Flandin, G., Dolan, R. J., & Frith, C. D.(2006). Dopamine-dependent prediction errors underpinreward-seeking behaviour in humans. Nature, 442(7106),1042e1045. http://dx.doi.org/10.1038/Nature05051.
Ramnani, N., & Owen, A. M. (2004). Anterior prefrontal cortex:insights into function from anatomy and neuroimaging.Nature Reviews Neuroscience, 5(3), 184e194. http://dx.doi.org/10.1038/nrn1343.
Samanez-Larkin, G. R., Hollon, N. G., Carstensen, L. L., &Knutson, B. (2008). Individual differences in insular sensitivityduring loss anticipation predict avoidance learning.Psychological Science, 19(4), 320e323. http://dx.doi.org/10.1111/j.1467-9280.2008.02087.x.
Schultz, W., Dayan, P., & Montague, P. R. (1997). A neural substrateof prediction and reward. Science, 275(5306), 1593e1599.
Seymour, B., Daw, N., Dayan, P., Singer, T., & Dolan, R. (2007).Differential encoding of losses and gains in the humanstriatum [Comparative Study Research Support, Non-U.S.Gov't] The Journal of Neuroscience: the Official Journal of the Societyfor Neuroscience, 27(18), 4826e4831. http://dx.doi.org/10.1523/JNEUROSCI.0400-07.2007.
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P.,Janavs, J., Weiller, E., et al. (1998). The Mini-InternationalNeuropsychiatric Interview (M.I.N.I.): the development andvalidation of a structured diagnostic psychiatric interview forDSM-IV and ICD-10. Journal of Clinical Psychiatry, 59(Suppl. 20),22e33. quiz 34e57.
Shin, N. Y., Jang, J. H., Kim, H. S., Shim, G., Hwang, J. Y., Kim, S. N.,et al. (2013). Impaired body but not face perception in patientswith obsessive-compulsive disorder [Research Support, Non-U.S. Gov't] Journal of Neuropsychology, 7(1), 58e71. http://dx.doi.org/10.1111/j.1748-6653.2012.02035.x.
Sjoerds, Z., de Wit, S., van den Brink, W., Robbins, T. W.,Beekman, A. T., Penninx, B. W., et al. (2013). Behavioral andneuroimaging evidence for overreliance on habit learning inalcohol-dependent patients. Translational Psychiatry, 3, e337.http://dx.doi.org/10.1038/tp.2013.107.
Slotnick, S. D., Moo, L. R., Segal, J. B., & Hart, J., Jr. (2003). Distinctprefrontal cortex activity associated with item memory andsource memory for visual shapes. Brain Research. CognitiveBrain Research, 17(1), 75e82.
Smittenaar, P., FitzGerald, T. H., Romei, V., Wright, N. D., &Dolan, R. J. (2013). Disruption of dorsolateral prefrontal cortexdecreases model-based in favor of model-free control inhumans. Neuron, 80(4), 914e919. http://dx.doi.org/10.1016/j.neuron.2013.08.009.
Stefanacci, L., & Amaral, D. G. (2002). Some observations oncortical inputs to the macaque monkey amygdala: ananterograde tracing study. Journal of Comparative Neurology,451(4), 301e323. http://dx.doi.org/10.1002/Cne.10339.
Talmi, D., Seymour, B., Dayan, P., & Dolan, R. J. (2008). Humanpavlovian-instrumental transfer. Journal of Neuroscience,28(2), 360e368. http://dx.doi.org/10.1523/JNEUROSCI.4028-07.2008.
Tanaka, S. C., Balleine, B. W., & O'Doherty, J. P. (2008). Calculatingconsequences: brain systems that encode the causal effects ofactions. Journal of Neuroscience, 28(26), 6750e6755. http://dx.doi.org/10.1523/Jneurosci.1808-08.2008.
Tricomi, E., Balleine, B. W., & O'Doherty, J. P. (2009). A specific rolefor posterior dorsolateral striatum in human habit learning.European Journal of Neuroscience, 29(11), 2225e2232. http://dx.doi.org/10.1111/j.1460-9568.2009.06796.x.
Valentin, V. V., Dickinson, A., & O'Doherty, J. P. (2007).Determining the neural substrates of goal-directed learning inthe human brain. Journal of Neuroscience, 27(15), 4019e4026.http://dx.doi.org/10.1523/Jneurosci.0564-07.2007.
Voon, V., Derbyshire, K., Ruck, C., Irvine, M. A., Worbe, Y.,Enander, J., et al. (2014). Disorders of compulsivity: a commonbias towards learning habits. Molecular Psychiatry. http://dx.doi.org/10.1038/mp.2014.44.
Whitfield-Gabrieli, S., & Nieto-Castanon, A. (2012). Conn: afunctional connectivity toolbox for correlated andanticorrelated brain networks. Brain Connectivity, 2(3), 125e141.http://dx.doi.org/10.1089/brain.2012.0073.
deWit, S., Watson, P., Harsay, H. A., Cohen, M. X., van de Vijver, I.,& Ridderinkhof, K. R. (2012). Corticostriatal connectivityunderlies individual differences in the balance betweenhabitual and goal-directed action control [RandomizedControlled Trial Research Support, Non-U.S. Gov't] Journal ofNeuroscience, 32(35), 12066e12075. http://dx.doi.org/10.1523/JNEUROSCI.1088-12.2012.
Wunderlich, K., Dayan, P., & Dolan, R. J. (2012). Mapping valuebased planning and extensively trained choice in thehuman brain [Research Support, Non-U.S. Gov't] NatureNeuroscience, 15(5), 786e791. http://dx.doi.org/10.1038/nn.3068.
Yin, H. H., Knowlton, B. J., & Balleine, B. W. (2004). Lesions ofdorsolateral striatum preserve outcome expectancy butdisrupt habit formation in instrumental learning. EuropeanJournal of Neuroscience, 19(1), 181e189.
Yin, H. H., Ostlund, S. B., Knowlton, B. J., & Balleine, B. W. (2005).The role of the dorsomedial striatum in instrumentalconditioning [Comparative Study Research Support, N.I.H.,Extramural Research Support, U.S. Gov't, Non-P.H.S. ResearchSupport, U.S. Gov't, P.H.S.] European Journal of Neuroscience,22(2), 513e523. http://dx.doi.org/10.1111/j.1460-9568.2005.04218.x.
Zhang, H., Hubbard, P. L., Parker, G. J., & Alexander, D. C. (2011).Axon diameter mapping in the presence of orientationdispersion with diffusion MRI. NeuroImage, 56(3), 1301e1315.http://dx.doi.org/10.1016/j.neuroimage.2011.01.084.
Zhang, H., Schneider, T., Wheeler-Kingshott, C. A., &Alexander, D. C. (2012). NODDI: practical in vivo neuriteorientation dispersion and density imaging of the humanbrain. NeuroImage, 61(4), 1000e1016. http://dx.doi.org/10.1016/j.neuroimage.2012.03.072.