Modulation of motivational salience processing during the early stages of psychosis

Schizophrenia Research

Volumn 166, Issue 1-3, 2014, Pages 17-23

  Smieskova, Renata ^a,c   Roiser, Jonathan P ^b   Chaddock, Christopher A ^e   Schmidt, André ^a,c   Harrisberger, Fabienne ^a,c   Bendfeldt, Kerstin ^c   Simon, Andor ^d   Walter, Anna ^a   Fusar Poli, Paolo ^e   McGuire, Philip K ^e   Lang, Undine E ^a   Riecher Rössler, Anita ^a   Borgwardt, Stefan ^a,c,e  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY HOSPITAL BASEL   (Switzerland)

^d Specialized Early Psychosis Outpatient Service for Adolescents and Young Adults   (Switzerland)

^e KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Antipsychotic medication; Cingulate cortex; Functional MRI; Insula

Indexed keywords

ANTIDEPRESSANT AGENT; ATYPICAL ANTIPSYCHOTIC AGENT; NEUROLEPTIC AGENT;

ADULT; ANTERIOR CINGULATE; ARTICLE; ASSOCIATION; BRAIN FUNCTION; CINGULATE GYRUS; CLINICAL ARTICLE; CONTROLLED STUDY; DELUSION; DISEASE SEVERITY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INFERIOR PARIETAL LOBULE; INSULA; MALE; MENTAL HEALTH; NEUROIMAGING; PREMOTOR CORTEX; PRIORITY JOURNAL; PSYCHOSIS; REWARD; SALIENCE; SOMATOSENSORY CORTEX; ACUTE DISEASE; BRAIN; BRAIN CIRCULATION; BRAIN MAPPING; DELUSIONS; DRUG EFFECTS; FOLLOW UP; HALLUCINATIONS; MOTIVATION; NEUROPSYCHOLOGICAL TEST; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PHYSIOLOGY; PROBABILITY; PRODROMAL SYMPTOM; PROSPECTIVE STUDY; PSYCHOTIC DISORDERS; YOUNG ADULT;

ACUTE DISEASE; ADULT; ANTIPSYCHOTIC AGENTS; BRAIN; BRAIN MAPPING; CEREBROVASCULAR CIRCULATION; DELUSIONS; FEMALE; FOLLOW-UP STUDIES; HALLUCINATIONS; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MOTIVATION; NEUROPSYCHOLOGICAL TESTS; PROBABILITY; PRODROMAL SYMPTOMS; PROSPECTIVE STUDIES; PSYCHOTIC DISORDERS; REWARD; YOUNG ADULT;

EID: 84948982597     PISSN: 09209964     EISSN: 15732509     Source Type: Journal    
DOI: 10.1016/j.schres.2015.04.036     Document Type: Article

References (65)

1. Abi-Dargham, A., Rodenhiser, J., Printz, D., Zea-Ponce, Y., Gil, R., Kegeles, L.S., Weiss, R., Cooper, T.B., Mann, J.J., Van Heertum, R.L., Gorman, J.M., Laruelle, M., 2000. Increased baseline occupancy of D2 receptors by dopamine in schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 97, 8104-8109.
2. Abi-Dargham, A., Xu, X., Thompson, J.L., Gil, R., Kegeles, L.S., Urban, N., Narendran, R., Hwang, D.R., Laruelle, M., Slifstein, M., 2012. Increased prefrontal cortical D1 receptors in drug naive patients with schizophrenia: a PET study with [11C]NNC112. J. Psychopharmacol. 26, 794-805.
3. Balthazar, M.L., Pereira, F.R., Lopes, T.M., da Silva, E.L., Coan, A.C., Campos, B.M., Duncan, N.W., Stella, F., Northoff, G., Damasceno, B.P., Cendes, F., 2014. Neuropsychiatric symptoms in Alzheimer's disease are related to functional connectivity alterations in the salience network. Hum. Brain Mapp. 35, 1237-1246.
4. Berridge, K.C., Robinson, T.E., 1998. What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res. Brain Res. Rev. 28, 309-369.
5. Charboneau, E.J., Dietrich, M.S., Park, S., Cao, A., Watkins, T.J., Blackford, J.U., Benningfield, M.M., Martin, P.R., Buchowski, M.S., Cowan, R.L., 2013. Cannabis cue-induced brain activation correlates with drug craving in limbic and visual salience regions, preliminary results. Psychiatry Res. 214, 122-131.
6. Connolly, C.G., Wu, J., Ho, T.C., Hoeft, F., Wolkowitz, O., Eisendrath, S., Frank, G., Hendren, R., Max, J.E., Paulus, M.P., Tapert, S.F., Banerjee, D., Simmons, A.N., Yang, T.T., 2013. Resting-state functional connectivity of subgenual anterior cingulate cortex in depressed adolescents. Biol. Psychiatry 74, 898-907.
7. Day, G.S., Farb, N.A., Tang-Wai, D.F., Masellis, M., Black, S.E., Freedman, M., Pollock, B.G., Chow, T.W., 2013. Salience network resting-state activity, prediction of frontotemporal dementia progression. JAMA Neurol. 70, 1249-1253.
8. Diaconescu, A.O., Jensen, J., Wang, H., Willeit, M., Menon, M., Kapur, S., McIntosh, A.R., 2011. Aberrant effective connectivity in schizophrenia patients during appetitive conditioning. Front. Hum. Neurosci. 4, 239.
9. Doll, A., Sorg, C., Manoliu, A., Wöller, A., Meng, C., Förstl, H., Zimmer, C., Wohlschläger, A.M., Riedl, V., 2013. Shifted intrinsic connectivity of central executive and salience network in borderline personality disorder. Front. Hum. Neurosci. 7, 727.
10. Eshel, N., Roiser, J.P., 2010. Reward and punishment processing in depression. Biol. Psychiatry 68, 118-124.
11. Esslinger, C., Englisch, S., Inta, D., Rausch, F., Schirmbeck, F., Mier, D., Kirsch, P., Meyer-Lindenberg, A., Zink, M., 2012. Ventral striatal activation during attribution of stimulus saliency and reward anticipation is correlated in unmedicated first episode schizophrenia patients. Schizophr. Res. 140, 114-121.
12. Exner, C., Weniger, G., Schmidt-Samoa, C., Irle, E., 2006. Reduced size of the presupplementary motor cortex and impaired motor sequence learning in firstepisode schizophrenia. Schizophr. Res. 84, 386-396.
13. Fusar-Poli, P., Broome, M.R., Matthiasson, P., Williams, S.C., Brammer, M., McGuire, P.K., 2007. Effects of acute antipsychotic treatment on brain activation in first episode psychosis: an fMRI study. Eur. Neuropsychopharmacol. 17, 492-500.
14. Fusar-Poli, P., Deste, G., Smieskova, R., Barlati, S., Yung, A.R., Howes, O., Stieglitz, R.D., Vita, A., McGuire, P., Borgwardt, S., 2012. Cognitive functioning in prodromal psychosis: a meta-analysis. Arch. Gen. Psychiatry 69, 562-571.
15. Fusar-Poli, P., Smieskova, R., Kempton, M.J., Ho, B.C., Andreasen, N.C., Borgwardt, S., 2013. Progressive brain changes in schizophrenia related to antipsychotic treatment? A meta-analysis of longitudinal MRI studies. Neurosci. Biobehav. Rev. 37, 1680-1691.
16. Gradin, V.B., Waiter, G., O'Connor, A., Romaniuk, L., Stickle, C., Matthews, K., Hall, J., Douglas Steele, J., 2013. Salience network-midbrain dysconnectivity and blunted reward signals in schizophrenia. Psychiatry Res. 211, 104-111.
17. Grimm, O., Vollstädt-Klein, S., Krebs, L., Zink, M., Smolka, M.N., 2012. Reduced striatal activation during reward anticipation due to appetite-provoking cues in chronic schizophrenia: a fMRI study. Schizophr. Res. 134, 151-157.
18. Ham, T., Leff, A., de Boissezon, X., Joffe, A., Sharp, D.J., 2013. Cognitive control and the salience network: an investigation of error processing and effective connectivity. J. Neurosci. 33, 7091-7098.
19. Hanakawa, T., Dimyan, M.A., Hallett, M., 2008. Motor planning, imagery, and execution in the distributed motor network: a time-course study with functional MRI. Cereb. Cortex 18, 2775-2788.
20. Heinz, A., Schlagenhauf, F., 2010. Dopaminergic dysfunction in schizophrenia: salience attribution revisited. Schizophr. Bull. 36, 472-485.
21. Ho, B.C., Andreasen, N.C., Ziebell, S., Pierson, R., Magnotta, V., 2011. Long-term antipsychotic treatment and brain volumes: a longitudinal study of first-episode schizophrenia. Arch. Gen. Psychiatry 68, 128-137.
22. Howes, O.D., Kapur, S., 2009. The dopamine hypothesis of schizophrenia: version III-the final common pathway. Schizophr. Bull. 35, 549-562.
23. Jensen, J., Kapur, S., 2009. Salience and psychosis:moving fromtheory to practise. Psychol. Med. 39, 197-198.
24. Juckel, G., Schlagenhauf, F., Koslowski, M., Filonov, D., Wüstenberg, T., Villringer, A., Knutson, B., Kienast, T., Gallinat, J., Wrase, J., Heinz, A., 2006a. Dysfunction of ventral striatal reward prediction in schizophrenic patients treated with typical, not atypical, neuroleptics. Psychopharmacol. (Berl.) 187, 222-228.
25. Juckel, G., Schlagenhauf, F., Koslowski, M., Wustenberg, T., Villringer, A., Knutson, B., Wrase, J., Heinz, A., 2006b. Dysfunction of ventral striatal reward prediction in schizophrenia. NeuroImage 29, 409-416.
26. Kapur, S., 2003. Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am. J. Psychiatry 160, 13-23.
27. 18F]fluorodopa study. Arch. Gen. Psychiatry 61, 134-142.
28. Moran, L.V., Tagamets, M.A., Sampath, H., O'Donnell, A., Stein, E.A., Kochunov, P., Hong, L.E., 2013. Disruption of anterior insula modulation of large-scale brain networks in schizophrenia. Biol. Psychiatry 74, 467-474.
29. 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., 2008. Substantia nigra/ventral tegmental reward prediction error disruption in psychosis. Mol. Psychiatry 13 (239), 267-276.
30. Nagy, H., Levy-Gigi, E., Somlai, Z., Takáts, A., Bereczki, D., Kéri, S., 2012. The effect of dopamine agonists on adaptive and aberrant salience in Parkinson's disease. Neuropsychopharmacology 37, 950-958.
31. Nielsen, M.O., Rostrup, E., Wulff, S., Bak, N., Broberg, B.V., Lublin, H., Kapur, S., Glenthoj, B., 2012. Improvement of brain reward abnormalities by antipsychotic monotherapy in schizophrenia. Arch. Gen. Psychiatry 69, 1195-1204.
32. Ojeda, N., Ortuño, F., Arbizu, J., López, P., Martí-Climent, J.M., Peñuelas, I., Cervera-Enguix, S., 2002. Functional neuroanatomy of sustained attention in schizophrenia: contribution of parietal cortices. Hum. Brain Mapp. 17, 116-130.
33. Ongür, D., Price, J.L., 2000. The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. Cereb. Cortex 10, 206-219.
34. Orliac, F., Naveau, M., Joliot, M., Delcroix, N., Razafimandimby, A., Brazo, P., Dollfus, S., Delamillieure, P., 2013. Links among resting-state default-mode network, salience network, and symptomatology in schizophrenia. Schizophr. Res. 148, 74-80.
35. Ortuño, F., Ojeda, N., Arbizu, J., López, P., Martí-Climent, J.M., Peñuelas, I., Cervera, S., 2002. Sustained attention in a counting task: normal performance and functional neuroanatomy. NeuroImage 17, 411-420.
36. Palaniyappan, L., Liddle, P.F., 2012. Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. J. Psychiatry Neurosci. 37, 17-27.
37. Palaniyappan, L., Simmonite, M., White, T.P., Liddle, E.B., Liddle, P.F., 2013. Neural primacy of the salience processing system in schizophrenia. Neuron 79, 814-828.
38. Pannekoek, J.N., Veer, I.M., van Tol, M.J., van der Werff, S.J., Demenescu, L.R., Aleman, A., Veltman, D.J., Zitman, F.G., Rombouts, S.A., van der Wee, N.J., 2013a. Aberrant limbic and salience network resting-state functional connectivity in panic disorder without comorbidity. J. Affect. Disord. 145, 29-35.
39. Pannekoek, J.N., Veer, I.M., van Tol, M.J., van der Werff, S.J., Demenescu, L.R., Aleman, A., Veltman, D.J., Zitman, F.G., Rombouts, S.A., van der Wee, N.J., 2013b. Resting-state functional connectivity abnormalities in limbic and salience networks in social anxiety disorder without comorbidity. Eur. Neuropsychopharmacol. 23, 186-195.
40. Pessiglione, M., Seymour, B., Flandin, G., Dolan, R.J., Frith, C.D., 2006. Dopaminedependent prediction errors underpin reward-seeking behaviour in humans. Nature 442, 1042-1045.
41. Petersson, K.M., Nichols, T.E., Poline, J.B., Holmes, A.P., 1999. Statistical limitations in functional neuroimaging. II. Signal detection and statistical inference. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 1261-1281.
42. Pujol, N., Penadés, R., Rametti, G., Catalán, R., Vidal-Piñeiro, D., Palacios, E., Bargallo, N., Bernardo, M., Junqué, C., 2013. Inferior frontal and insular cortical thinning is related to dysfunctional brain activation/deactivation during working memory task in schizophrenic patients. Psychiatry Res. 214, 94-101.
43. Radua, J., Borgwardt, S., Crescini, A., Mataix-Cols, D., Meyer-Lindenberg, A., McGuire, P.K., Fusar-Poli, P., 2012. Multimodal meta-analysis of structural and functional brain changes in first episode psychosis and the effects of antipsychotic medication. Neurosci. Biobehav. Rev. 36, 2325-2333.
44. Radua, J., Del Pozo, N.O., Gómez, J., Guillen-Grima, F., Ortuño, F., 2014. Meta-analysis of functional neuroimaging studies indicates that an increase of cognitive difficulty during executive tasks engages brain regions associated with time perception. Neuropsychologia 58, 14-22.
45. Rausch, F., Eifler, S., Esser, A., Esslinger, C., Schirmbeck, F., Meyer-Lindenberg, A., Zink, M., 2013. The Early Recognition Inventory ERIraos detects at riskmental states of psychosis with high sensitivity. Compr. Psychiatry 54, 1068-1076.
46. Riecher-Rössler, A., Gschwandtner, U., Aston, J., Borgwardt, S., Drewe, M., Fuhr, P., Pflüger, M., Radü, W., Schindler, C., Stieglitz, R.D., 2007. The Basel early-detection-ofpsychosis (FEPSY)-study-design and preliminary results. Acta Psychiatr. Scand. 115, 114-125.
47. Riecher-Rossler, A., Pflueger, M.O., Aston, J., Borgwardt, S.J., Brewer, W.J., Gschwandtner, U., Stieglitz, R.D., 2009. Efficacy of using cognitive status in predicting psychosis: a 7-year follow-up. Biol. Psychiatry 66, 1023-1030.
48. Roiser, J.P., Stephan, K.E., den Ouden, H.E., Barnes, T.R., Friston, K.J., Joyce, E.M., 2009. Do patients with schizophrenia exhibit aberrant salience? Psychol. Med. 39, 199-209.
49. Roiser, J.P., Stephan, K.E., den Ouden, H.E., Friston, K.J., Joyce, E.M., 2010. Adaptive and aberrant reward prediction signals in the human brain. NeuroImage 50, 657-664.
50. Roiser, J.P., Howes, O.D., Chaddock, C.A., Joyce, E.M., McGuire, P., 2013. Neural and behavioral correlates of aberrant salience in individuals at risk for psychosis. Schizophr. Bull. 39, 1328-1336.
51. Schlagenhauf, F., Juckel, G., Koslowski, M., Kahnt, T., Knutson, B., Dembler, T., Kienast, T., Gallinat, J., Wrase, J., Heinz, A., 2008. Reward system activation in schizophrenic patients switched from typical neuroleptics to olanzapine. Psychopharmacol. (Berl.) 196, 673-684.
52. Schmidt, A., Smieskova, R., Aston, J., Simon, A., Allen, P., Fusar-Poli, P., McGuire, P.K., Riecher-Rössler, A., Stephan, K.E., Borgwardt, S., 2013. Brain connectivity abnormalities predating the onset of psychosis: correlation with the effect of medication. JAMA Psychiatry 70, 903-912.
53. Simon, A.E., Borgwardt, S., Riecher-Rössler, A., Velthorst, E., de Haan, L., Fusar-Poli, P., 2013. Moving beyond transition outcomes: meta-analysis of remission rates in individuals at high clinical risk for psychosis. Psychiatry Res. 209, 266-272.
54. Smieskova, R., Fusar-Poli, P., Allen, P., Bendfeldt, K., Stieglitz, R.D., Drewe, J., Radue, E.W., McGuire, P.K., Riecher-Roessler, A., Borgwardt, S.J., 2009. The effects of antipsychotics on the brain:what havewe learnt fromstructural imaging of schizophrenia?-a systematic review. Curr. Pharm. Des. 15, 2535-2549.
55. Smieskova, R., Fusar-Poli, P., Riecher-Rössler, A., Borgwardt, S., 2012. Neuroimaging and resilience factors-staging of the at-risk mental state? Curr. Pharm. Des. 18, 416-421.
56. Snitz, B.E., MacDonald, A., Cohen, J.D., Cho, R.Y., Becker, T., Carter, C.S., 2005. Lateral and medial hypofrontality in first-episode schizophrenia: functional activity in a medication-naive state and effects of short-term atypical antipsychotic treatment. Am. J. Psychiatry 162, 2322-2329.
57. Sullivan, E.V., Müller-Oehring, E., Pitel, A.L., Chanraud, S., Shankaranarayanan, A., Alsop, D.C., Rohlfing, T., Pfefferbaum, A., 2013. A selective insular perfusion deficit contributes to compromised salience network connectivity in recovering alcoholic men. Biol. Psychiatry 74, 547-555.
58. Uddin, L.Q., Supekar, K., Lynch, C.J., Khouzam, A., Phillips, J., Feinstein, C., Ryali, S., Menon, V., 2013. Salience network-based classification and prediction of symptom severity in children with autism. JAMA Psychiatry 70, 869-879.
59. 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., 2009. Patients with schizophrenia have a reduced neural response to both unpredictable and predictable primary reinforcers. Neuropsychopharmacology 34, 1567-1577.
60. White, T.P., Joseph, V., Francis, S.T., Liddle, P.F., 2010. Aberrant salience network (bilateral insula and anterior cingulate cortex) connectivity during information processing in schizophrenia. Schizophr. Res. 123, 105-115.
61. White, T.P., Gilleen, J., Shergill, S.S., 2013. Dysregulated but not decreased salience network activity in schizophrenia. Front. Hum. Neurosci. 7, 65.
62. Winton-Brown, T.T., Fusar-Poli, P., Ungless, M.A., Howes, O.D., 2014. Dopaminergic basis of salience dysregulation in psychosis. Trends Neurosci. 37, 85-94.
63. Wotruba, D., Michels, L., Buechler, R., Metzler, S., Theodoridou, A., Gerstenberg, M., Walitza, S., Kollias, S., Rössler, W., Heekeren, K., 2014. Aberrant coupling within and across the default mode, task-positive, and salience network in subjects at risk for psychosis. Schizophr. Bull. 40 (5), 1095-1104.
64. Yung, A.R., Phillips, L.J., McGorry, P.D., McFarlane, C.A., Francey, S., Harrigan, S., Patton, G.C., Jackson, H.J., 1998. Prediction of psychosis. A step towards indicated prevention of schizophrenia. Br. J. Psychiatry Suppl. 172, 14-20.
65. Yung, A.R., Yuen, H.P., McGorry, P.D., Phillips, L.J., Kelly, D., Dell'Olio, M., Francey, S.M., Cosgrave, E.M., Killackey, E., Stanford, C., Godfrey, K., Buckby, J., 2005. Mapping the onset of psychosis: the Comprehensive Assessment of At-Risk Mental States. Aust. NZ J. Psychiatry 39, 964-971.