Skip to main content
Log in

Social Cognition in Chiari Malformation Type I: a Preliminary Characterization

  • Original Paper
  • Published:
The Cerebellum Aims and scope Submit manuscript

Abstract

Chiari malformation type I (CM-I) is a neurological disorder in which cerebellar tonsils are herniated through the foramen magnum into the spinal canal. A wide spectrum of cognitive deficits underlying this pathology has been reported, but the literature about social cognition is insufficient. Clinical research has pointed out the cerebellar role in Theory of Mind (ToM), indicating that there are several disorders with cerebellar pathology that reveal a poorer performance in social cognition tasks. The main purpose of this study is to compare the performance on ToM tasks between CM-I patients and healthy controls. The protocol includes Faux Pas test, Happé’s Strange Stories test, Ice-Cream Van task, the FEEL test, and the Word Accentuation Test. In order to eliminate the possible influence of covariables, physical pain and anxious-depressive symptomatology have been controlled for. According to the results, CM-I patients performed worse than matched healthy controls on ToM tasks, except for facial emotion recognition. These differences remained even after controlling for the neuropsychiatric variables and physical pain. Thus, it can be suggested that patients with CM-I are impaired in their social skills related to their performance on ToM tasks. These findings can be considered to be a preliminary approach to the specific study of social cognition in relation to CM-I since it is similar to other cerebellar pathologies and to previous literature on the cerebellum’s role in social cognition.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Hoche F, Guell X, Sherman JC, Vangel MG, Schmahmann JD. Cerebellar contribution to social cognition. Cerebellum. 2016;15(6):732–43. https://doi.org/10.1007/s12311-015-0746-9.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Van Overwalle F, D’aes T, Mariën P. Social cognition and the cerebellum: a meta-analytic connectivity analysis. Hum Brain Mapp. 2015;36(12):5137–54. https://doi.org/10.1002/hbm.23002.

    Article  PubMed  Google Scholar 

  3. Tirapu J, Pérez G, Erekatxo M, Pelegrín C. ¿Qué es la teoría de la mente? Rev Neurol. 2007;44(8):479–89.

    Google Scholar 

  4. Abu-Akel A. A neurobiological mapping of theory of mind. Brain Res Rev. 2003;43(1):29–40. https://doi.org/10.1016/S0165-0173(03)00190-5.

    Article  PubMed  Google Scholar 

  5. Clausi S, Olivito G, Lupo M, Siciliano L, Bozzali M, Leggio M. The cerebellar predictions for social interactions: theory of mind abilities in patients with degenerative cerebellar atrophy. Front Cell Neurosci. 2019;12(510):1–16. https://doi.org/10.3389/fncel.2018.00510.

    Article  Google Scholar 

  6. 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. https://doi.org/10.1080/17470919.2015.1005666.

    Article  PubMed  Google Scholar 

  7. Van Overwalle F, Mariën P. Functional connectivity between the cerebrum and cerebellum in social cognition: a multi-study analysis. Neuroimage. 2016;124(Pt A):248–55. https://doi.org/10.1016/j.neuroimage.2015.09.001.

    Article  PubMed  Google Scholar 

  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. https://doi.org/10.1016/j.neuroimage.2013.09.033.

    Article  PubMed  Google Scholar 

  9. Manto M, Mariën P. Schmahmann’s syndrome—identification of the third cornerstone of clinical ataxiology. Cerebellum Ataxias. 2015;2(2):1–5. https://doi.org/10.1186/s40673-015-0023-1.

    Article  Google Scholar 

  10. Schamahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(4):561–79.

    Article  Google Scholar 

  11. Schmahmann JD, Weilburg JB, Sherman JC. The neuropsychiatry of the cerebellum—insights from the clinic. Cerebellum. 2007;6(3):254–67. https://doi.org/10.1080/14734220701490995.

    Article  PubMed  Google Scholar 

  12. Garrard P, Martin NH, Giunti P, Cipolotti L. Cognitive and social cognitive functioning in spinocerebellar ataxia. J Neurol. 2008;255(3):398–405. https://doi.org/10.1007/s00415-008-0680-6.

    Article  CAS  PubMed  Google Scholar 

  13. Sokolovsky N, Cook A, Hunt H, Giunti P, Cipolotti L. A preliminary characterization of cognition and social cognition in spinocerebellar ataxia types 2, 1 and 7. Behav Neurol. 2010;23(1–2):17–29. https://doi.org/10.3233/BEN-2010-0270.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. D’Agata F, Caroppo P, Baudino B, Caglio M, Croce M, Bergui M, et al. The recognition of facial emotions in spinocerebellar ataxia patients. Cerebellum. 2011;10(3):600–10. https://doi.org/10.1007/s12311-011-0276-z.

    Article  CAS  PubMed  Google Scholar 

  15. Costabile T, Capretti V, Abate F, Liguori A, Paciello F, Pane C, et al. Emotion recognition and psychological comorbidity in Friedreich’s ataxia. Cerebellum. 2018;17(3):336–45. https://doi.org/10.1007/s12311-018-0918-5.

    Article  PubMed  Google Scholar 

  16. Tubbs RS, Oakes WJ. Introduction and classification of the Chiari malformations. In: Tubbs RS, Oakes WJ, editors. The Chiari malformations; 2013. p. 1–3. https://doi.org/10.1007/978-1-4614-6369-6_2.

    Chapter  Google Scholar 

  17. Rogers JM, Savage G, Stoodley MA. A systematic review of cognition in Chiari I malformation. Neuropsychol Rev. 2018;28(2):176–87. https://doi.org/10.1007/s11065-018-9368-6.

    Article  PubMed  Google Scholar 

  18. García M, Lázaro E, López-Paz JF, Martínez O, Pérez M, Berrocoso S, et al. Cognitive functioning in Chiari malformation type I without posterior fossa surgery. Cerebellum. 2018a;17(5):564–74. https://doi.org/10.1007/s12311-018-0940-7.

    Article  PubMed  Google Scholar 

  19. García M, Amayra I, Lázaro E, López-Paz JF, Martínez O, Pérez M, et al. Comparison between decompressed and non-decompressed Chiari malformation type I patients: a neuropsychological study. Neuropsychologia. 2018b;121:135–43. https://doi.org/10.1016/j.neuropsychologia.2018.11.002.

    Article  PubMed  Google Scholar 

  20. Houston JR, Hughes ML, Lien MC, Martin BA, Loth F, Luciano MG, et al. An electrophysiological study of cognitive and emotion processing in type I Chiari malformation. Cerebellum. 2018;17(4):404–18. https://doi.org/10.1007/s12311-018-0923-8.

    Article  CAS  PubMed  Google Scholar 

  21. García, M.A., Allen, P.A., Li, X., Houston, J.R., Loth, F., Labuda, R., & Delahanty, D.L. (2019). An examination of pain, disability, and the psychological correlates of Chiari malformation pre- and post-surgical correction. Disabil Health J. Advanced online publication doi: https://doi.org/10.1016/j.dhjo.2019.05.004.

  22. Lázaro E, García M, Amayra I, López-Paz JF, Martínez O, Pérez M, et al. Anxiety and depression in Chiari malformation. J Integr Neurosci. 2018;17(4):343–8. https://doi.org/10.31083/j.jin.2018.04.0414.

    Article  Google Scholar 

  23. Stone VE, Baron-Cohen S, Knight RT. Frontal lobe contributions to theory of mind. J Cogn Neurosci. 1998;10:640–56.

    Article  CAS  PubMed  Google Scholar 

  24. Serrano, C. (2018). Faux Pas test (adult)—Español. [Web page] retrieved from http://www.autismresearchcentre.com/arc_tests. Accessed October 2017

  25. Happé F. An advanced test of theory of mind: understanding of story characters’ thoughts and feelings by able autistic, mentally handicapped, and normal children and adults. J Autism Dev Disord. 1994;24:129–54.

    Article  PubMed  Google Scholar 

  26. Pousa E (2002) Measurement of theory of mind in healthy adolescents: translation and cultural adaptation of F. Happé’s theory of mind stories (1999). (Doctoral thesis, Autonomous University of Barcelona, Spain).

  27. Perner J, Wimmer H. “John thinks that Mary thinks that….”: attribution of second-order beliefs by 5- to 10-year-old children. J Exp Child Psychol. 1985;39(3):437–71. https://doi.org/10.1016/0022-0965(85)90051-7.

    Article  Google Scholar 

  28. Montoya MM, Molina-Cobos FJ. Evaluación de relaciones deícticas y teoría de la mente con una muestra de estudiantes universitarios. Int J Psychol Psychol Ther. 2015;15(2):191–203.

    Google Scholar 

  29. Kessler H, Bayerl P, Deighton RM, Traue HC. Facially expressed emotion labeling (FEEL): PC-gestützer test zur emotions erkennung. Verhaltenstherapie und Verhaltensmedizin. 2002;23(3):297–306.

    Google Scholar 

  30. Lázaro E, Amayra I, López-Paz JF, Martínez O, Pérez M, Berrocoso S, et al. Instrument for assessing the ability to identify emotional facial expressions in healthy children and in children with ADHD: the FEEL test. J Atten Disord. 2016:1–7. https://doi.org/10.1177/1087054716682335.

  31. Nelson HE, O’Conell A. Dementia: the estimation of premorbid intelligence levels using the new adult reading test. Cortex. 1978;14:234–44.

    Article  CAS  PubMed  Google Scholar 

  32. Del Ser T, González-Montalvo JI, Martínez-Espinosa S, Delgado-Villapalos C, Bermejo F. Estimation of premorbid intelligence in Spanish people with the word accentuation test and its application to the diagnosis of dementia. Brain Cogn. 1997;33(3):343–56. https://doi.org/10.1006/brcg.1997.0877.

    Article  PubMed  Google Scholar 

  33. Zigmond A, Snaith R. The hospital anxiety and depression scale. Acta Psychiatr Scand. 1983;67:361–70.

    Article  CAS  Google Scholar 

  34. Herrero MJ, Blanch J, Peri JM, De Pablo J, Pintor L, Bulbena A. A validation study of the hospital anxiety and depression scale (HADS) in a Spanish population. Gen Hosp Psychiatry. 2003;25(3):277–83.

    Article  CAS  PubMed  Google Scholar 

  35. Jacobson GP, Ramadan NM, Aggarwal SK, Newman CW. The Henry Ford hospital headache disability inventory (HDI). Neurology. 1994;44(5):837–42.

    Article  CAS  PubMed  Google Scholar 

  36. Rodríguez L, Cano FJ, Blanco A. Conductas de dolor y discapacidad en migrañas y cefaleas tensionales. Adaptación española del pain behavior questionnaire (PBQ) y del headache disability inventory (HDI). Análisis y Modificación de Conducta. 2000;26(109):739–62.

    Google Scholar 

  37. Vernon H, Mior S. The neck disability index: a study of reliability and validity. J Manipulative Physiol Ther. 1991;14(7):409–15.

    CAS  PubMed  Google Scholar 

  38. Andrade JA, Delgado AD, Almécija R. Validation of the Spanish version of the neck disability index. Spine. 2010;35(4):114–8. https://doi.org/10.1097/BRS.0b013e3181afea5d.

    Article  Google Scholar 

  39. Fairbank JC, Couper J, Davies JB, O’Brien JP. The Oswestry low back pain questionnaire. Physiotherapy. 1980;66(8):271–3.

    CAS  PubMed  Google Scholar 

  40. Flórez MT, García MA, García F, Armenteros J, Álvarez A, Martínez MD. Adaptación transcultural a la población española de la escala de incapacidad por dolor lumbar de Oswestry. Rehabilitación. 1995;29:138–45.

    Google Scholar 

  41. Oakley BFM, Brewer R, Bird G, Catmur C. Theory of mind is not theory of emotion: a cautionary note on the reading the mind in the eyes test. J Abnorm Psychol. 2016;125(6):818–23. https://doi.org/10.1037/abn0000182.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Guell X, Gabrieli JDE, Schmahmann JD. Embodied cognition and the cerebellum: perspectives from the dysmetria of thought and the universal cerebellar transform theories. Cortex. 2018;100:140–8. https://doi.org/10.1016/j.cortex.2017.07.005.

    Article  PubMed  Google Scholar 

  43. Olivito G, Clausi S, Laghi F, Tedesco AM, Baiocco R, Mastropasqua C, et al. Resting-state functional connectivity changes between dentate nucleus and cortical social brain regions in autism spectrum disorders. Cerebellum. 2017;16(2):283–92. https://doi.org/10.1007/s12311-016-0795-8.

    Article  PubMed  Google Scholar 

  44. Laird AR, Fox PM, Eickhoff SB, Turner JA, Ray KI, McKay DR, et al. Behavioral interpretations of intrinsic connectivity networks. J Cogn Neurosci. 2011;23(12):4022–37. https://doi.org/10.1162/jocn_a_00077.

    Article  PubMed  PubMed Central  Google Scholar 

  45. Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106(5):2322–22345. https://doi.org/10.1152/jn.00339.2011.

    Article  PubMed  PubMed Central  Google Scholar 

  46. Kurtcan S, Alkan A, Yetis H, Tuzu U, Aralasmak A, Toprak H, et al. Diffusion tensor imaging findings of the brainstem in subjects with tonsillar ectopia. Acta Neurol Belg. 2018;118(1):39–45. https://doi.org/10.1007/s13760-017-0792-9.

    Article  PubMed  Google Scholar 

  47. Kumar M, Rathore RK, Srivastava A, Yadav SK, Behari S, Gupta RK. Correlation of diffusion tensor imaging metrics with neurocognitive function in Chiari I malformation. World Neurosurg. 2011;76(1–2):189–94. https://doi.org/10.1016/j.wneu.2011.02.022.

    Article  PubMed  Google Scholar 

  48. Leggio M, Olivito G. Topography of the cerebellum in relation to social brain regions and emotions. Handb Clin Neurol. 2018;154:71–84. https://doi.org/10.1016/B978-0-444-63956-1.00005-9.

    Article  PubMed  Google Scholar 

  49. Mar RA. The neural bases of social cognition and story comprehension. Annu Rev Psychol. 2011;62:103–34. https://doi.org/10.1146/annurev-psych-120709-145406.

    Article  PubMed  Google Scholar 

  50. Van Overwalle F, Heleven E, Ma N, Mariën P. Tell me twice: a multi-study analysis of the functional connectivity between the cerebrum and cerebellum after repeated trait information. Neuroimage. 2017;144(Pt a):241–52. https://doi.org/10.1016/j.neuroimage.2016.08.046.

    Article  PubMed  Google Scholar 

  51. Van Overwalle F, De Coninck S, Heleven E, Perrotta G, Taib NOB, Manto M, et al. The role of the cerebellum in reconstructing social action sequences: a pilot study. Soc Cogn Affect Neurosci. 2019;14(5):549–58. https://doi.org/10.1093/scan/nsz032.

    Article  PubMed  PubMed Central  Google Scholar 

  52. Heleven E, van Dun K, Van Overvalle F. The posterior cerebellum is involved in constructing social action sequences: an fMRI study. Sci Rep. 2019;9(1):1–11. https://doi.org/10.1038/s41598-019-46962-7.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank ChySPA and all of the participants for their involvement in the study and their effort.

Funding

This study was funded by a grant from the Education Department of the Basque Government’s ‘Programa Predoctoral de Formación de Personal Investigador No Doctor’ (PRE_2016_1_0099 to Maitane García).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Maitane García.

Ethics declarations

Conflict of Interest

The co-authors declare that they have no conflict of interest.

Ethical Approval and Informed Consent

All procedures performed in this study were developed in accordance with the ethical standards and with the 1964 Helsinki declaration and its later amendments. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

García, M., Amayra, I., López-Paz, J.F. et al. Social Cognition in Chiari Malformation Type I: a Preliminary Characterization. Cerebellum 19, 392–400 (2020). https://doi.org/10.1007/s12311-020-01117-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-020-01117-7

Keywords

Navigation