Hostname: page-component-7479d7b7d-767nl Total loading time: 0 Render date: 2024-07-11T01:43:44.199Z Has data issue: false hasContentIssue false
  • English
  • Français

Empathy and aversion: the neural signature of mentalizing in Tourette syndrome

Published online by Cambridge University Press:  25 October 2016

C. M. Eddy ,
A. E. Cavanna  and
P. C. Hansen
C. M. Eddy*
Affiliation:
BSMHFT National Centre for Mental Health, Birmingham, UK College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
A. E. Cavanna
Affiliation:
BSMHFT National Centre for Mental Health, Birmingham, UK College of Medical and Dental Sciences, University of Birmingham, Birmingham, UK
P. C. Hansen
Affiliation:
Birmingham University Imaging Centre and School of Psychology, College of Life and Environmental Sciences, University of Birmingham, UK
*
*Address for correspondence: Dr C. M. Eddy, Senior Research Fellow in Neuropsychiatry, Research and Innovation, The Barberry, 25 Vincent Drive, Edgbaston, Birmingham B15 2FG, UK. (Email: clare.eddy@bsmhft.nhs.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Previous studies suggest that adults with Tourette syndrome (TS) can respond unconventionally on tasks involving social cognition. We therefore hypothesized that these patients would exhibit different neural responses to healthy controls in response to emotionally salient expressions of human eyes.

Method

Twenty-five adults with TS and 25 matched healthy controls were scanned using fMRI during the standard version of the Reading the Mind in the Eyes Task which requires mental state judgements, and a novel comparison version requiring judgements about age.

Results

During prompted mental state recognition, greater activity was apparent in TS within left orbitofrontal cortex, posterior cingulate, right amygdala and right temporo-parietal junction (TPJ), while reduced activity was apparent in regions including left inferior parietal cortex. Age judgement elicited greater activity in TS within precuneus, medial prefrontal and temporal regions involved in mentalizing. The interaction between group and task revealed differential activity in areas including right inferior frontal gyrus. Task-related activity in the TPJ covaried with global ratings of the urge to tic.

Conclusions

While recognizing mental states, adults with TS exhibit greater activity than controls in brain areas involved in the processing of negative emotion, in addition to reduced activity in regions associated with the attribution of agency. In addition, increased recruitment of areas involved in mental state reasoning is apparent in these patients when mentalizing is not a task requirement. Our findings highlight differential neural reactivity in response to emotive social cues in TS, which may interact with tic expression.

Keywords

Emotionsocial cognitiontheory of mindticsTourette syndrome
Type
Original Articles
Information
Psychological Medicine , Volume 47 , Issue 3 , February 2017 , pp. 507 - 517
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albin, RL, Mink, JW (2006). Recent advances in Tourette syndrome research. Trends in Neurosciences 29, 175–182.CrossRefGoogle ScholarPubMed
Allison, T, Puce, A, McCarthy, G (2000). Social perception from visual cues: role of the STS region. Trends in Cognitive Sciences 4, 267–278.Google Scholar
APA (2000). Diagnostic and Statistical Manual of Mental Disorders: Text Revision; DSM-IV-TR, 4th edn. American Psychiatric Association: Washington, DC.Google Scholar
Aron, AR, Robbins, TW, Poldrack, RA (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences 8, 170–177.CrossRefGoogle ScholarPubMed
Aron, AR, Robbins, TW, Poldrack, RA (2014). Inhibition and the right inferior frontal cortex: one decade on. Trends in Cognitive Sciences 18, 177–185.Google Scholar
Baron-Cohen, S, Wheelwright, S, Hill, J, Raste, Y, Plumb, I (2001). The ‘Reading the Mind in the Eyes’ Test revised version: a study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry 42, 241–251.Google Scholar
Bertolino, A, Arciero, G, Rubino, V, Latorre, V, De Candia, M, Mazzola, V, Blasi, G, Caforio, G, Hariri, A, Kolachana, B, Nardini, M, Weinberger, DR, Scarabino, T (2005). Variation of human amygdala response during threatening stimuli as a function of 5′HTTLPR genotype and personality style. Biological Psychiatry 57, 1517–1525.Google Scholar
Brown, MR, Lebel, RM, Dolcos, F, Wilman, AH, Silverstone, PH, Pazderka, H, Fujiwara, E, Wild, TC, Carroll, AM, Hodlevskyy, O, Zedkova, L, Zwaigenbaum, L, Thompson, AH, Greenshaw, AJ, Dursun, SM (2012). Effects of emotional context on impulse control. Neuroimage 63, 434–446.Google Scholar
Cavanna, AE, Rickards, H (2013). The psychopathological spectrum of Gilles de la Tourette syndrome. Neuroscience and Biobehavioral Reviews 37, 1008–1015.CrossRefGoogle ScholarPubMed
Cavanna, AE, Trimble, MR (2006). The precuneus: a review of its functional anatomy and behavioural correlates. Brain 129, 564–583.CrossRefGoogle ScholarPubMed
Cerri, G, Cabinio, M, Blasi, V, Borroni, P, Iadanza, A, Fava, E, Fornia, L, Ferpozzi, V, Riva, M, Casarotti, A, Martinelli Boneschi, F, Falini, A, Bello, L (2015). The mirror neuron system and the strange case of Broca's area. Human Brain Mapping 36, 1010–1027.Google Scholar
Cheng, Y, Chen, C, Lin, CP, Chou, KH, Decety, J (2010). Love hurts: an fMRI study. Neuroimage 51, 923–929.Google Scholar
Christenson, GA, Faber, RJ, deZwaan, M (1994). Compulsive buying: descriptive characteristics and psychiatric comorbidity. Journal of Clinical Psychiatry 55, 5–11.Google Scholar
Cox, RW (1996). AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research 29, 16273.CrossRefGoogle ScholarPubMed
Dehning, S, Burger, MB, Krause, D, Jobst, A, Yundina, E, Müller, N, Meyer, S, Zill, P, Buchheim, A (2015). Tourette syndrome is associated with insecure attachment and higher aggression. International Journal of Neuroscience 125, 521–525.Google Scholar
Eddy, CM (2016). The junction between self and other? Temporo-parietal dysfunction in neuropsychiatry. Neuropsychologia 89, 465–477.CrossRefGoogle ScholarPubMed
Eddy, CM, Cavanna, AE (2013 a). On being your own worst enemy: an investigation of non-obscene socially inappropriate symptoms in Tourette syndrome. Journal of Psychiatric Research 47, 1259–1263.Google Scholar
Eddy, CM, Cavanna, AE (2013 b). Altered social cognition in Tourette syndrome: nature and Implications. Behavioural Neurology 7, 15–22.Google Scholar
Eddy, CM, Cavanna, AE (2015). Triangles, tricks and tics: Hyper-mentalizing in response to animated shapes in Tourette syndrome. Cortex 71, 68–75.Google Scholar
Eddy, CM, Cavanna, AE, Rickards, HE, Hansen, PC (2016). Temporo-parietal dysfunction in Tourette syndrome: insights from an fMRI study of Theory of Mind. Journal of Psychiatric Research 81, 102–111.Google Scholar
Eddy, CM, Macerollo, A, Martino, D, Cavanna, AE (2015). Interpersonal reactivity differences in Tourette syndrome. Psychiatry Research 228, 932–935.Google Scholar
Eddy, CM, Mitchell, IJ, Beck, SR, Cavanna, AE, Rickards, HE (2010 a). Altered attribution of intention in Tourette syndrome. Journal of Neuropsychiatry and Clinical Neurosciences 22, 348–351.Google Scholar
Eddy, CM, Mitchell, IJ, Beck, SR, Cavanna, AE, Rickards, HE (2010 b). Impaired comprehension of nonliteral language in Tourette Syndrome. Cognitive and Behavioral Neurology 23, 178–184.Google Scholar
Eddy, CM, Mitchell, IJ, Beck, SR, Cavanna, AE, Rickards, H (2011). Social reasoning in Tourette syndrome. Cognitive Neuropsychiatry 16, 326–347.CrossRefGoogle ScholarPubMed
Gallagher, HL, Frith, CD (2003). Functional imaging of ‘theory of mind’. Trends in Cognitive Sciences 7, 77–83.Google Scholar
Harris, LT, Fiske, ST (2007). Social groups that elicit disgust are differentially processed in mPFC. Social Cognitive and Affective Neuroscience 2, 45–51.Google Scholar
Jenkinson, M, Bannister, P, Brady, M, Smith, S (2002). Improved optimisation for the robust and accurate linear registration and motion correction of brain images. NeuroImage 172, 825–841.Google Scholar
Johnstone, T, Ores Walsh, KS, Greischar, LL, Alexander, AL, Fox, AS, Davidson, RJ, Oakes, TR (2006). Motion correction and the use of motion covariates in multiple-subject fMRI analysis. Human Brain Mapping 27, 779–788.Google Scholar
Kurlan, R, Daragjati, C, Como, PG, McDermott, MP, Trinidad, KS, Roddy, S, Brower, CA, Robertson, MM (1996). Non-obscene complex socially inappropriate behavior in Tourette's syndrome. Journal of Neuropsychiatry and Clinical Neurosciences 8, 311–317.Google Scholar
Leckman, JF, Riddle, MA, Hardin, M, Ort, SI, Swartz, KL, Stevenson, J, Cohen, DJ (1989). The Yale global tic severity scale: initial testing of a clinician-rated scale of tic severity. Journal of the American Academy of Child and Adolescent Psychiatry 28, 566–573.Google Scholar
Lissek, S, Peters, S, Fuchs, N, Witthaus, H, Nicolas, V, Tegenthoff, M, Juckel, G, Brüne, M (2008). Cooperation and deception recruit different subsets of the theory-of-mind network. PLoS ONE 3, e2023.Google Scholar
Mitchell, DGV, Luo, Q, Mondillo, K, Vythilingam, M, Finger, EC, Blair, RJR (2008). The interference of operant task performance by emotional distracters: an antagonistic relationship between the amygdala and frontoparietal cortices. Neuroimage 40, 859–868.Google Scholar
Moor, BG, Macks, ZA, Güroglu, B, Rombouts, SA, Molen, MW, Crone, EA (2012). Neurodevelopmental changes of reading the mind in the eyes. Social Cognitive and Affective Neuroscience 7, 44–52.Google Scholar
Neuner, I, Kellermann, T, Stöcker, T, Kircher, T, Habel, U, Shah, JN, Schneider, F (2010). Amygdala hypersensitivity in response to emotional faces in Tourette's patients. World Journal of Biological Psychiatry 11, 858–872.Google Scholar
Oakley, BF, Brewer, R, Bird, G, Catmur, C (2016). Theory of mind is not theory of emotion: a cautionary note on the Reading the Mind in the Eyes Test. Journal of Abnormal Psychology 125, 818–823.Google Scholar
Pegna, AJ, Khateb, A, Lazeyras, F, Seghier, ML (2005). Discriminating emotional faces without primary visual cortices involves the right amygdala. Nature Neuroscience 8, 24–25.Google Scholar
Robertson, MM, Eapen, V (1996). The National Hospital Interview schedule for the assessment of Gilles de la Tourette syndrome and related behaviours. International Journal of Methods in Psychiatry Research 6, 203–226.3.3.CO;2-F>CrossRefGoogle Scholar
Roelofs, K, Minelli, A, Mars, RB, van Peer, J, Toni, I (2009). On the neural control of social emotional behavior. Social Cognitive and Affective Neuroscience 4, 50–58.CrossRefGoogle ScholarPubMed
Ruby, P, Decety, J (2001). Effect of subjective perspective taking during simulation of action: a PET investigation of agency. Nature Neuroscience 4, 546–550.Google Scholar
Schurz, M, Radua, J, Aichhorn, M, Richlan, F, Perner, J (2014). Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neuroscience and Biobehavioral Reviews 42, 9–34.Google Scholar
Scharf, JM, Miller, LL, Mathews, CA, Ben-Shlomo, Y (2012). Prevalence of tourette syndrome and chronic tics in the population based Avon longitudinal study of parents and children cohort. Journal of the American Academy of Child and Adolescent Psychiatry 51, 192–201.Google Scholar
Schoenbaum, G, Chiba, AA, Gallagher, M (1998). Orbitofrontal cortex and basolateral amygdala encode expected outcomes during learning. Nature Neuroscience 1, 155–159.Google Scholar
Sharp, C, Pane, H, Ha, C, Venta, A, Patel, AB, Sturek, J, Fonagy, P (2011). Theory of mind and emotion regulation difficulties in adolescents with borderline traits. Journal of the American Academy of Child and Adolescent Psychiatry 50, 563–573.Google Scholar
Smith, SM, Jenkinson, M, Woolrich, MW, Beckmann, CF, Behrens, TE, Johansen-Berg, H, Bannister, PR, De Luca, M, Drobnjak, I, Flitney, DE, Niazy, RK, Saunders, J, Vickers, J, Zhang, Y, De Stefano, N, Brady, JM, Matthews, PM (2004). Advances in functional and structural MR image analysis and implementation as FSL. NeuroImage 23 (S1), 208–219.CrossRefGoogle ScholarPubMed
Sommer, IE, Aleman, A, Somers, M, Boks, MP, Kahn, RS (2008). Sex differences in handedness, asymmetry of the planum temporale and functional language lateralization. Brain Research 1206, 76–88.Google Scholar
Sprengelmeyer, R, Rausch, M, Eysel, UT, Przuntek, H (1998). Neural structures associated with recognition of facial expressions of basic emotions. Proceedings of the Royal Society of London, Series B: Biological Sciences 265, 1927–1931.Google Scholar
Storch, EA, Larson, MJ, Goodman, WK, Rasmussen, SA, Price, LH, Murphy, TK (2010). Development and psychometric evaluation of the yale-brown obsessive-compulsive scale second edition. Psychological Assessment 22, 223–232.Google Scholar
Sugiura, M, Wakusawa, K, Sekiguchi, A, Sassa, Y, Jeong, H, Horie, K, Sato, S, Kawashima, R (2009). Extraction of situational meaning by integrating multiple meanings in a complex environment: a functional MRI study. Human Brain Mapping 30, 2676–2688.Google Scholar
Thibert, AL, Day, HI, Sandor, P (1995). Self-concept and self-consciousness in adults with Tourette syndrome. Canadian Journal of Psychiatry 40, 35–39.Google Scholar
Tseng, LY, Tseng, P, Liang, WK, Hung, DL, Tzeng, OJ, Muggleton, NG, Juan, CH (2014). The role of superior temporal sulcus in the control of irrelevant emotional face processing: a transcranial direct current stimulation study. Neuropsychologia 64, 124–133.Google Scholar
Wagenbreth, C, Rieger, J, Heinze, HJ, Zaehle, T (2014). Seeing emotions in the eyes – inverse priming effects induced by eyes expressing mental states. Frontiers in Psychology 5, 1039.Google Scholar
Wang, Z, Maia, TV, Marsh, R, Colibazzi, T, Gerber, A, Peterson, BS (2011). The neural circuits that generate tics in Tourette's syndrome. American Journal of Psychiatry 168, 1326–1337.CrossRefGoogle ScholarPubMed
Wicker, B, Keysers, C, Plailly, J, Royet, JP, Gallese, V, Rizzolatti, G (2003). Both of us disgusted in my insula: the common neural basis of seeing and feeling disgust. Neuron 40, 655–664.Google Scholar
Woods, DW, Piacentini, J, Himle, MB, Chang, S (2005). Premonitory Urge for Tics Scale (PUTS): initial psychometric results and examination of the premonitory urge phenomenon in youths with tic disorders. Journal of Developmental and Behavioral Pediatrics 26, 397–403.CrossRefGoogle ScholarPubMed
Supplementary material: File

Eddy supplementary material

Eddy supplementary material

Download Eddy supplementary material(File)
File 4.3 MB