Emotion and Theory of Mind in Schizophrenia—Investigating the Role of the Cerebellum

Cerebellum

Volumn 15, Issue 3, 2016, Pages 357-368

  Mothersill, Omar ^a,b   Knee Zaska, Charlotte ^a,b   Donohoe, Gary ^a,b  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

^b TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

Cerebellum; Emotion; Neuroimaging; Schizophrenia; Social cognition

Indexed keywords

BOLD SIGNAL; BRAIN BLOOD FLOW; CEREBELLUM; CEREBELLUM VERMIS; COGNITIVE DEFECT; DISEASE SEVERITY; EMOTION; FACIAL RECOGNITION; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; FUSIFORM GYRUS; HUMAN; INFERIOR TEMPORAL GYRUS; LEFT HEMISPHERE; LINGUAL GYRUS; POSITRON EMISSION TOMOGRAPHY; PRIORITY JOURNAL; REVIEW; RIGHT HEMISPHERE; SCHIZOPHRENIA; SOCIAL COGNITION; SYSTEMATIC REVIEW; THEORY OF MIND; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY;

CEREBELLUM; EMOTIONS; FUNCTIONAL NEUROIMAGING; HUMANS; SCHIZOPHRENIA; SCHIZOPHRENIC PSYCHOLOGY; THEORY OF MIND;

EID: 84936862252     PISSN: 14734222     EISSN: 14734230     Source Type: Journal    
DOI: 10.1007/s12311-015-0696-2     Document Type: Review

References (81)

1. Van Overwalle F. Social cognition and the brain: a meta‐analysis. Hum Brain Mapp. 2009;30(3):829–58.
2. Couture SM, Penn DL, Roberts DL. The functional significance of social cognition in schizophrenia: a review. Schizophr Bull. 2006;32 suppl 1:S44–63.
3. Fett A-KJ, Viechtbauer W, Dominguez M-d-G, Penn DL, van Os J, Krabbendam L. The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: a meta-analysis. Neurosci Biobehav Rev. 2011;35(3):573–88.
4. Brady LS, Insel TR. Translating discoveries into medicine: psychiatric drug development in 2011. Neuropsychopharmacol Off Publ Am Coll Neuropsychopharmacol. 2012;37(1):281–3.
5. Insel T, Cuthbert B, Garvey M, Heinssen R, Pine DS, Quinn K, et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am J Psychiatr. 2010;167(7):748–51.
6. Walter H, Schnell K, Erk S, Arnold C, Kirsch P, Esslinger C, et al. Effects of a genome-wide supported psychosis risk variant on neural activation during a theory-of-mind task. Mol Psychiatry. 2011;16(4):462–70.
7. Dannlowski U, Stuhrmann A, Beutelmann V, Zwanzger P, Lenzen T, Grotegerd D, et al. Limbic scars: long-term consequences of childhood maltreatment revealed by functional and structural magnetic resonance imaging. Biol Psychiatry. 2012;71(4):286–93.
8. Van Overwalle F, Baetens K, Mariën P, Vandekerckhove M. Social cognition and the cerebellum: a meta-analysis of over 350 fMRI studies. Neuroimage. 2014;86:554–72.
9. Kohler CG, Walker JB, Martin EA, Healey KM, Moberg PJ. Facial emotion perception in schizophrenia: a meta-analytic review. Schizophr Bull. 2010;36(5):1009–19.
10. Aleman A, Kahn RS. Strange feelings: do amygdala abnormalities dysregulate the emotional brain in schizophrenia? Prog Neurobiol. 2005;77(5):283–98.
11. Gur R, Nimgaonkar V, Almasy L, Calkins M, Ragland J, Pogue-Geile M, et al. Neurocognitive endophenotypes in a multiplex multigenerational family study of schizophrenia. Am J Psychiatr. 2007;164(5):813–9.
12. Aghevli MA, Blanchard JJ, Horan WP. The expression and experience of emotion in schizophrenia: a study of social interactions. Psychiatry Res. 2003;119(3):261–70.
13. Goldman AI, Margolis E, Samuels R, Stich S. Theory of mind. Oxford handbook of philosophy and cognitive science. Oxford: Oxford University Press; 2012:402-24.
14. Schnell K, Bluschke S, Konradt B, Walter H. Functional relations of empathy and mentalizing: an fMRI study on the neural basis of cognitive empathy. Neuroimage. 2011;54(2):1743–54.
15. Csibra G. Goal attribution to inanimate agents by 6.5-month-old infants. Cognition. 2008;107(2):705–17.
16. Nuechterlein KH, Barch DM, Gold JM, Goldberg TE, Green MF, Heaton RK. Identification of separable cognitive factors in schizophrenia. Schizophr Res. 2004;72(1):29–39.
17. McGurk SR, Twamley EW, Sitzer DI, McHugo GJ, Mueser KT. A meta-analysis of cognitive remediation in schizophrenia. Am J Psychiatry. 2007;164(12):1791–802.
18. Lewandowski KE, Cohen BM, Keshavan MS, Öngür D. Relationship of neurocognitive deficits to diagnosis and symptoms across affective and non-affective psychoses. Schizophr Res. 2011;133(1):212–7.
19. Baddeley A. Working memory. Science. 1992;255(5044):556–9.
20. Süß H-M, Oberauer K, Wittmann WW, Wilhelm O, Schulze R. Working-memory capacity explains reasoning ability—and a little bit more. Intelligence. 2002;30(3):261–88.
21. Baddeley A. Working memory and language: an overview. J Commun Disord. 2003;36(3):189–208.
22. Colom R, Rebollo I, Palacios A, Juan-Espinosa M, Kyllonen PC. Working memory is (almost) perfectly predicted by g. Intelligence. 2004;32(3):277–96.
23. Bühner M, Kröner S, Ziegler M. Working memory, visual-spatial-intelligence and their relationship to problem-solving. Intelligence. 2008;36(6):672–80.
24. Colom R, Abad FJ, Quiroga MÁ, Shih PC, Flores-Mendoza C. Working memory and intelligence are highly related constructs, but why? Intelligence. 2008;36(6):584–606.
25. Thach WT, Goodkin H, Keating J. The cerebellum and the adaptive coordination of movement. Annu Rev Neurosci. 1992;15(1):403–42.
26. Bostan AC, Dum RP, Strick PL. Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci. 2013;17(5):241–54.
27. Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatry Clin Neurosci. 2004;16(3):367–78.
28. Baillieux H, De Smet HJ, Dobbeleir A, Paquier PF, De Deyn PP, Mariën P. Cognitive and affective disturbances following focal cerebellar damage in adults: a neuropsychological and SPECT study. Cortex. 2010;46(7):869–79.
29. Manto M, Mariën P. Schmahmann’s syndrome—identification of the third cornerstone of clinical ataxiology. Cerebellum Ataxias. 2015;2(2):1–5.
30. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(4):561–79.
31. Tavano A, Grasso R, Gagliardi C, Triulzi F, Bresolin N, Fabbro F, et al. Disorders of cognitive and affective development in cerebellar malformations. Brain. 2007;130(10):2646–60.
32. Stoodley CJ, Schmahmann JD. Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage. 2009;44(2):489–501.
33. Van Overwalle, F, Baetens, K, Mariën, P, Vandekerckhove, M. Cerebellar areas dedicated to Social Cognition? A comparison of meta-analytic and connectivity results. Soc Neurosci 2015; 10(4):337-44.
34. Riedel MC, Ray KL, Dick AS, Sutherland MT, Hernandez Z, Fox PM, et al. Meta-analytic connectivity and behavioral parcellation of the human cerebellum. Neuroimage. 2015;117:327–42.
35. Turner BM, Paradiso S, Marvel CL, Pierson R, Boles Ponto LL, Hichwa RD, et al. The cerebellum and emotional experience. Neuropsychologia. 2007;45(6):1331–41.
36. Krienen FM, Buckner RL. Segregated fronto-cerebellar circuits revealed by intrinsic functional connectivity. Cereb Cortex. 2009;19(10):2485–97.
37. O'Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cereb Cortex. 2010;20(4):953–65.
38. Buckner R, Krienen F, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:2322–45.
39. Andreasen NC, O'Leary DS, Cizadlo T, Arndt S, Rezai K, Ponto L, et al. Schizophrenia and cognitive dysmetria: a positron-emission tomography study of dysfunctional prefrontal-thalamic-cerebellar circuitry. Proc Natl Acad Sci. 1996;93(18):9985–90.
40. Crespo‐Facorro B, Wiser AK, Andreasen NC, O'Leary DS, Watkins GL, Boles Ponto LL, et al. Neural basis of novel and well‐learned recognition memory in schizophrenia: a positron emission tomography study. Hum Brain Mapp. 2001;12(4):219–31.
41. Walter H, Vasic N, Höse A, Spitzer M, Wolf RC. Working memory dysfunction in schizophrenia compared to healthy controls and patients with depression: evidence from event-related fMRI. Neuroimage. 2007;35(4):1551–61.
42. Müller JL, Röder C, Schuierer G, Klein HE. Subcortical overactivation in untreated schizophrenic patients: a functional magnetic resonance image finger‐tapping study. Psychiatry Clin Neurosci. 2002;56(1):77–84.
43. Volkow ND, Levy A, Brodie JD, Wolf AP, Cancro R, Van Gelder P, et al. Low cerebellar metabolism in medicated patients with chronic schizophrenia. Am J Psychiatry. 1992;149:686–8.
44. Liu H, Fan G, Xu K, Wang F. Changes in cerebellar functional connectivity and anatomical connectivity in schizophrenia: a combined resting‐state functional MRI and diffusion tensor imaging study. J Magn Reson Imaging. 2011;34(6):1430–8.
45. Friston KJ, Frith CD. Schizophrenia: a disconnection syndrome? Clin Neurosci. 1995;3(2):89–97.
46. Tran KD, Smutzer GS, Doty RL, Arnold SE. Reduced Purkinje cell size in the cerebellar vermis of elderly patients with schizophrenia. Am J Psychiatr. 1998;155(9):1288–90.
47. Okugawa G, Nobuhara K, Sugimoto T, Kinoshita T. Diffusion tensor imaging study of the middle cerebellar peduncles in patients with schizophrenia. Cerebellum. 2005;4(2):123–7.
48. Kyriakopoulos M, Vyas NS, Barker GJ, Chitnis XA, Frangou S. A diffusion tensor imaging study of white matter in early-onset schizophrenia. Biol Psychiatry. 2008;63(5):519–23.
49. Wassink TH, Andreasen NC, Nopoulos P, Flaum M. Cerebellar morphology as a predictor of symptom and psychosocial outcome in schizophrenia. Biol Psychiatry. 1999;45(1):41–8.
50. Pedersen A, Koelkebeck K, Brandt M, Wee M, Kueppers KA, Kugel H, et al. Theory of mind in patients with schizophrenia: is mentalizing delayed? Schizophr Res. 2012;137(1):224–9.
51. Lakis N, Jiménez JA, Mancini-Marïe A, Stip E, Lavoie ME, Mendrek A. Neural correlates of emotional recognition memory in schizophrenia: effects of valence and arousal. Psychiatry Res Neuroimaging. 2011;194(3):245–56.
52. Mendrek A, Jiménez J, Mancini-Marïe A, Fahim C, Stip E. Correlations between sadness-induced cerebral activations and schizophrenia symptoms: an fMRI study of sex differences. Eur Psychiatry. 2011;26(5):320–6.
53. Surguladze SA, Chu EM, Marshall N, Evans A, Anilkumar AP, Timehin C, et al. Emotion processing in schizophrenia: fMRI study of patients treated with risperidone long-acting injections or conventional depot medication. J Psychopharmacol. 2011;25(6):722–33.
54. Mendrek A, Mancini-Marië A, Fahim C, Stip E. Sex differences in the cerebral function associated with processing of aversive stimuli by schizophrenia patients. Aust N Z J Psychiatry. 2007;41(2):136–41.
55. Stip E, Fahim C, Liddle P, Mancini-Marïe A, Mensour B, Bentaleb LA, et al. Neural correlates of sad feelings in schizophrenia with and without blunted affect. Can J Psychiatr. 2005;50:909–17.
56. Brunet E, Sarfati Y, Hardy-Baylé M-C, Decety J. Abnormalities of brain function during a nonverbal theory of mind task in schizophrenia. Neuropsychologia. 2003;41(12):1574–82.
57. Mothersill O, Morris DW, Kelly S, Rose EJ, Bokde A, Reilly R, et al. Altered medial prefrontal activity during dynamic face processing in schizophrenia spectrum patients. Schizophr Res. 2014;157(1-3):225–30.
58. Andreasen NC, Calage CA, O'Leary DS. Theory of mind and schizophrenia: a positron emission tomography study of medication-free patients. Schizophr Bull. 2008;34(4):708–19.
59. Paradiso S, Andreasen NC, Crespo-Facorro B, O’Leary DS, Watkins GL, Ponto LLB, et al. Emotions in unmedicated patients with schizophrenia during evaluation with positron emission tomography. Am J Psychiatr. 2003;160(10):1775–83.
60. Crespo-Facorro B, Paradiso S, Andreasen NC, O'Leary DS, Watkins GL, Ponto LL, et al. Neural mechanisms of anhedonia in schizophrenia: a PET study of response to unpleasant and pleasant odors. JAMA. 2001;286(4):427–35.
61. Taylor SF, Phan KL, Britton JC, Liberzon I. Neural response to emotional salience in schizophrenia. Neuropsychopharmacol Off Publ Am College Neuropsychopharmacol. 2005;30(5):984–95.
62. Takahashi H, Koeda M, Oda K, Matsuda T, Matsushima E, Matsuura M, et al. An fMRI study of differential neural response to affective pictures in schizophrenia. Neuroimage. 2004;22(3):1247–54.
63. Fahim C, Stip E, Mancini-Marı̈e A, Beauregard M. Genes and memory: the neuroanatomical correlates of emotional memory in monozygotic twin discordant for schizophrenia. Brain Cogn. 2004;55(2):250–3.
64. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 2005;25(4):1325–35.
65. Eickhoff SB, Heim S, Zilles K, Amunts K. Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage. 2006;32(2):570–82.
66. Eickhoff SB, Paus T, Caspers S, Grosbras M-H, Evans AC, Zilles K, et al. Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage. 2007;36(3):511–21.
67. Diedrichsen J, Balsters JH, Flavell J, Cussans E, Ramnani N. A probabilistic MR atlas of the human cerebellum. Neuroimage. 2009;46(1):39–46.
68. Eickhoff SB, Laird AR, Grefkes C, Wang LE, Zilles K, Fox PT. Coordinate‐based activation likelihood estimation meta‐analysis of neuroimaging data: a random‐effects approach based on empirical estimates of spatial uncertainty. Hum Brain Mapp. 2009;30(9):2907–26.
69. Turkeltaub PE, Eickhoff SB, Laird AR, Fox M, Wiener M, Fox P. Minimizing within‐experiment and within‐group effects in activation likelihood estimation meta‐analyses. Hum Brain Mapp. 2012;33(1):1–13.
70. Eickhoff SB, Bzdok D, Laird AR, Kurth F, Fox PT. Activation likelihood estimation revisited. Neuroimage. 2012;59(3):2349–61.
71. Laird AR, Fox M, Price CJ, Glahn DC, Uecker AM, Lancaster JL, et al. ALE meta‐analysis: controlling the false discovery rate and performing statistical contrasts. Hum Brain Mapp. 2005;25(1):155–64.
72. Andreasen NC, Pierson R. The role of the cerebellum in schizophrenia. Biol Psychiatry. 2008;64(2):81–8.
73. Demirtas-Tatlidede A, Freitas C, Cromer JR, Safar L, Ongur D, Stone WS, et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res. 2010;124(1):91–100.
74. Stevens JS, Hamann S. Sex differences in brain activation to emotional stimuli: a meta-analysis of neuroimaging studies. Neuropsychologia. 2012;50(7):1578–93.
75. Singer T, Seymour B, O'Doherty J, Kaube H, Dolan RJ, Frith CD. Empathy for pain involves the affective but not sensory components of pain. Science. 2004;303(5661):1157–62.
76. Stephan KE, Friston KJ, Frith CD. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophr Bull. 2009;35(3):509–27.
77. Meyer-Lindenberg A, Poline JB, Kohn PD, Holt JL, Egan MF, Weinberger DR, et al. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am J Psychiatry. 2001;158(11):1809–17.
78. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR, et al. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch Gen Psychiatry. 2005;62(4):379–86.
79. Lawrie SM, Buechel C, Whalley HC, Frith CD, Friston KJ, Johnstone EC. Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biol Psychiatry. 2002;51(12):1008–11.
80. Breakspear M, Terry JR, Friston KJ, Harris AW, Williams LM, Brown K, et al. A disturbance of nonlinear interdependence in scalp EEG of subjects with first episode schizophrenia. Neuroimage. 2003;20(1):466–78.
81. Das P, Kemp AH, Flynn G, Harris AW, Liddell BJ, Whitford TJ, et al. Functional disconnections in the direct and indirect amygdala pathways for fear processing in schizophrenia. Schizophr Res. 2007;90(1):284–94.