Salience network-midbrain dysconnectivity and blunted reward signals in schizophrenia

Psychiatry Research - Neuroimaging

Volumn 211, Issue 2, 2013, Pages 104-111

  Gradin, Victoria B ^a   Waiter, Gordon ^b   O'Connor, Akira ^c   Romaniuk, Liana ^d   Stickle, Catriona ^e   Matthews, Keith ^a   Hall, Jeremy ^d   Douglas Steele, J ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c UNIVERSITY OF ST ANDREWS   (United Kingdom)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e ROYAL CORNHILL HOSPITAL   (United Kingdom)

Author keywords

Connectivity; Functional magnetic resonance imaging (fMRI); Midbrain; Reward processing; Salience network; Schizophrenia

Indexed keywords

ADULT; AMYGDALOID NUCLEUS; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN REGION; CLINICAL ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GUSTATORY CORTEX; HIPPOCAMPUS; HUMAN; INSULA; MALE; MESENCEPHALON; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; RETROSPLENIAL CORTEX; REWARD; SCHIZOPHRENIA; TEMPORAL LOBE;

ADULT; CEREBRAL CORTEX; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MALE; MESENCEPHALON; NEURAL PATHWAYS; REWARD; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY;

EID: 84873447602     PISSN: 09254927     EISSN: 18727506     Source Type: Journal    
DOI: 10.1016/j.pscychresns.2012.06.003     Document Type: Article

References (41)

1. Beck A.T., Ward H.C., Mendelson M. An inventory for measuring depression. Archives of General Psychiatry 1961, 4:561-571.
2. Berridge K.C. The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology 2007, 191:391-431.
3. Brett, M., Anton, J., Valabregue, R., Poline, J., 2002. Region of interest analysis using an SPM toolbox, In: Eighth International Conference on Functional Mapping of the Human Brain, Sendai, Japan.
4. Calhoun V.D., Eichele T., Pearlson G. Functional brain networks in schizophrenia: a review. Frontiers in Human Neuroscience 2009, 3:17.
5. Cohen M.X., Elger C.E., Weber B. Amygdala tractography predicts functional connectivity and learning during feedback-guided decision-making. NeuroImage 2008, 39:1396-1407.
6. Corlett P.R., Murray G.K., Honey G.D., Aitken M.R., Shanks D.R., Robbins T.W., Bullmore E.T., Dickinson A., Fletcher P.C. Disrupted prediction-error signal in psychosis: evidence for an associative account of delusions. Brain 2007, 130:2387-2400.
7. Dosenbach N.U., Fair D.A., Miezin F.M., Cohen A.L., Wenger K.K., Dosenbach R.A., 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. Proceedings of the National Academy of Sciences of the United States of America 2007, 104:11073-11078.
8. Glahn D.C., Laird A.R., Ellison-Wright I., Thelen S.M., Robinson J.L., Lancaster J.L., Bullmore E., Fox P.T. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biological Psychiatry 2008, 64:774-781.
9. Guillin O., Abi-Dargham A., Laruelle M. Neurobiology of dopamine in schizophrenia. International Review of Neurobiology 2007, 78:1-39.
10. Heinz A., Schlagenhauf F. Dopaminergic dysfunction in schizophrenia: salience attribution revisited. Schizophrenia Bulletin 2010, 36:472-485.
11. Juckel G., Schlagenhauf F., Koslowski M., Filonov D., Wustenberg T., Villringer A., Knutson B., Kienast T., Gallinat J., Wrase J., Heinz A. Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacology 2006, 187:222-228.
12. Juckel G., Schlagenhauf F., Koslowski M., Wustenberg T., Villringer A., Knutson B., Wrase J., Heinz A. Dysfunction of ventral striatal reward prediction in schizophrenia. NeuroImage 2006, 29:409-416.
13. Kahnt T., Park S.Q., Cohen M.X., Beck A., Heinz A., Wrase J. Dorsal striatal-midbrain connectivity in humans predicts how reinforcements are used to guide decisions. Journal of Cognitive Neuroscience 2009, 21:1332-1345.
14. Kapur S. Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. American Journal of Psychiatry 2003, 160:13-23.
15. Kay S.R., Fiszbein A., Opler L.A. The Positive and Negative Syndrome Scale (PANSS) for schizophrenia. Schizophrenia Bulletin 1987, 13:261-276.
16. 2O PET study. American Journal of Psychiatry 2003, 160:919-923.
17. Koch K., Schachtzabel C., Wagner G., Schikora J., Schultz C., Reichenbach J.R., Sauer H., Schlosser R.G. Altered activation in association with reward-related trial-and-error learning in patients with schizophrenia. NeuroImage 2010, 50:223-232.
18. Lawrie S.M., Buechel C., Whalley H.C., Frith C.D., Friston K.J., Johnstone E.C. Reduced fronto-temporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry 2002, 51:1008-1011.
19. Maldjian J.A., Laurienti P.J., Kraft R.A., Burdette J.H. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. NeuroImage 2003, 19:1233-1239.
20. Menon V., Uddin L.Q. Saliency, switching, attention and control: a network model of insula function. Brain Structure and Function 2010, 214:655-667.
21. Montague P.R., Dayan P., Sejnowski T.J. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. Journal of Neuroscience 1996, 16:1936-1947.
22. Murray G.K. The emerging biology of delusions. Psychological Medicine 2011, 41:7-13.
23. Murray G.K., Corlett P.R., Clark L., Pessiglione M., Blackwell A.D., Honey G., Jones P.B., Bullmore E.T., Robbins T.W., Fletcher P.C. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Molecular Psychiatry 2008, 12:46-77.
24. O'Doherty J.P., Dayan P., Friston K., Critchley H., Dolan R.J. Temporal difference models and reward-related learning in the human brain. Neuron 2003, 38:329-337.
25. Palaniyappan L., Liddle P.F. Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. Journal of Psychiatry and Neuroscience 2011, 36:100176.
26. Pettersson-Yeo W., Allen P., Benetti S., McGuire P., Mechelli A. Dysconnectivity in schizophrenia: where are we now?. Neuroscience and Biobehavioral Reviews 2011, 35:1110-1124.
27. Roiser J.P., Stephan K.E., den Ouden H.E., Barnes T.R., Friston K.J., Joyce E.M. Do patients with schizophrenia exhibit aberrant salience?. Psychological Medicine 2009, 39:199-209.
28. Romaniuk L., Honey G.D., King J.R., Whalley H.C., McIntosh A.M., Levita L., Hughes M., Johnstone E.C., Day M., Lawrie S.M., Hall J. Midbrain activation during Pavlovian conditioning and delusional symptoms in schizophrenia. Archives of General Psychiatry 2010, 67:1246-1254.
29. Schlagenhauf F., Sterzer P., Schmack K., Ballmaier M., Rapp M., Wrase J., Juckel G., Gallinat J., Heinz A. Reward feedback alterations in unmedicated schizophrenia patients: relevance for delusions. Biological Psychiatry 2009, 65:1032-1039.
30. Schultz W. Predictive reward signal of dopamine neurons. Journal of Neurophysiology 1998, 80:1-27.
31. Schultz W., Tremblay L., Hollerman J.R. Reward prediction in primate basal ganglia and frontal cortex. Neuropharmacology 1998, 37:421-429.
32. 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. Journal of Neuroscience 2007, 27:2349-2356.
33. Slotnick S.D., Moo L.R., Segal J.B., Hart J. Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. Brain Research. Cognitive Brain Research 2003, 17:75-82.
34. Spence S.A., Liddle P.F., Stefan M.D., Hellewell J.S., Sharma T., Friston K.J., Hirsch S.R., Frith C.D., Murray R.M., Deakin J.F., Grasby P.M. Functional anatomy of verbal fluency in people with schizophrenia and those at genetic risk. Focal dysfunction and distributed disconnectivity reappraised. British Journal of Psychiatry 2000, 176:52-60.
35. Spielberger, C.D., 1983. State-Trait Anxiety Inventory for Adults, STAI Form Y-1, Mind Garden, Palo Alto, CA.
36. Stephan K.E., Friston K.J., Frith C.D. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bulletin 2009, 35:509-527.
37. Taylor K.S., Seminowicz D.A., Davis K.D. Two systems of resting state connectivity between the insula and cingulate cortex. Human Brain Mapping 2009, 30:2731-2745.
38. Vincent J.L., Snyder A.Z., Fox M.D., Shannon B.J., Andrews J.R., Raichle M.E., Buckner R.L. Coherent spontaneous activity identifies a hippocampal-parietal memory network. Journal of Neurophysiology 2006, 96:3517-3531.
39. Waltz J.A., Schweitzer J.B., Gold J.M., Kurup P.K., Ross T.J., Salmeron B.J., Rose E.J., McClure S.M., Stein E.A. Patients with schizophrenia have a reduced neural response to both unpredictable and predictable primary reinforcers. Neuropsychopharmacology 2009, 34:1567-1577.
40. Wylie K.P., Tregellas J.R. The role of the insula in schizophrenia. Schizophrenia Research 2010, 123:93-104.
41. Zhou Y., Liang M., Tian L., Wang K., Hao Y., Liu H., Liu Z., Jiang T. Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophrenia Research 2007, 97:194-205.