Skip to main content

Advertisement

SpringerLink
Log in

Emotion Recognition and Psychological Comorbidity in Friedreich’s Ataxia

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

Abstract

Friedreich’s ataxia (FRDA) is an autosomal recessive disease presenting with ataxia, corticospinal signs, peripheral neuropathy, and cardiac abnormalities. Little effort has been made to understand the psychological and emotional burden of the disease. The aim of our study was to measure patients’ ability to recognize emotions using visual and non-verbal auditory hints, and to correlate this ability with psychological, neuropsychological, and neurological variables. We included 20 patients with FRDA, and 20 age, sex, and education matched healthy controls (HC). We measured emotion recognition using the Geneva Emotion Recognition Test (GERT). Neuropsychological status was assessed measuring memory, executive functions, and prosopagnosia. Psychological tests were Patient Health Questionnaire-9 (PHQ-9), State Trait Anxiety Inventory–state/−trait (STAI-S/−T), and Structured Clinical Interview for DSM Disorders II. FRDA patients scored worse at the global assessment and showed impaired immediate visuospatial memory and executive functions. Patients presented lower STAI-S scores, and similar scores at the STAI-T, and PHQ-9 as compared to HC. Three patients were identified with personality disorders. Emotion recognition was impaired in FRDA with 29% reduction at the total GERT score (95% CI − 44.8%, − 12.6%; p < 0.001; Cohen’s d = 1.2). Variables associated with poor GERT scores were the 10/36 spatial recall test, the Ray Auditory Verbal Learning Test, the Montreal Cognitive Assessment, and the STAI-T (R2 = 0.906; p < 0.001). FRDA patients have impaired emotion recognition that may be secondary to neuropsychological impairment. Depression and anxiety were not higher in FRDA as compared to HC and should not be considered as part of the disease.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Mayer J, Di Paolo M, Salovey P. Perceiving affective content in ambiguous visual stimuli: a component of emotional intelligence. J Pers Assess. 1990;54(3-4):772–81. https://doi.org/10.1080/00223891.1990.9674037.

    Article  PubMed  CAS  Google Scholar 

  2. Friedman HS. The relative strength of verbal versus nonverbal cues. Personal Soc Psychol Bull. 1978;4(1):147–50. https://doi.org/10.1177/014616727800400132.

    Article  Google Scholar 

  3. Bateson G, Jackson DD, Haley J, Weakland JH. Verso una teoria della schizophrenia. In: Bateson G, editor. Verso un'ecologia della mente. Milano: Adelphi; 1972.

    Google Scholar 

  4. Pollack IF, Polinko P, Albright AL. Mutism and pseudobulbar symptoms after resection of posterior fossa tumors in children: incidence and pathophysiology. Neurosurgery. 1995;37(5):885–93. https://doi.org/10.1227/00006123-199511000-00006.

    Article  PubMed  CAS  Google Scholar 

  5. Laible DJ, Thompson RA. Attachment and emotional understanding in preschool children. Dev Psychol. 1998;34(5):1038–45. https://doi.org/10.1037/0012-1649.34.5.1038.

    Article  PubMed  CAS  Google Scholar 

  6. Fox NA, Campos JJ. The development of emotion regulation: biological and behavioral considerations. Chicago: Society for Research in Child Development; 1994.

    Google Scholar 

  7. Rosen HJ, Pace-Savitsky K, Perry RJ, Kramer JH, Miller BL, Levenson RW. Recognition of emotion in the frontal and temporal variants of frontotemporal dementia. Dement Geriatr Cogn Disord. 2004;17(4):277–81. https://doi.org/10.1159/000077154.

    Article  PubMed  Google Scholar 

  8. Spoletini I, Marra C, Di Iulio F. Facial emotion recognition deficit in amnestic mild cognitive impairment and Alzheimer disease. Am J Geriatr Psychiatry. 2008;16(5):389–98. https://doi.org/10.1097/JGP.0b013e318165dbce.

    Article  PubMed  Google Scholar 

  9. Lavenu I, Pasquier F. Perception of emotion on faces in frontotemporal dementia and Alzheimer’s disease: a longitudinal study. Dement Geriatr Cogn Disord. 2005;19(1):37–41. https://doi.org/10.1159/000080969.

    Article  PubMed  CAS  Google Scholar 

  10. Sprengelmeyer R, Young AW, Calder AJ, Karnat A, Lange H, Hömberg V, et al. Loss of disgust: perception of faces and emotions in Huntington’s disease. Brain. 1996;119(5):1647–65. https://doi.org/10.1093/brain/119.5.1647.

  11. Streit M, Ioannides A, Sinnemann T, Wölwer W, Dammers J, Zilles K, et al. Disturbed facial affect recognition in patients with schizophrenia associated with hypoactivity in distributed brain regions: a magnetoencephalography study. Am J Psychiatr. 2001;158(9):1429–36. https://doi.org/10.1176/appi.ajp.158.9.1429.

  12. Seiferth NY, Pauly K, Habel U, Kellermann T, Shah NJ, Ruhrmann S, et al. Increased neural response related to neutral faces in individuals at risk for psychosis. NeuroImage. 2008;40(1):289–97. https://doi.org/10.1016/j.neuroimage.2007.11.020.

    Article  PubMed  Google Scholar 

  13. Kosaka H, Omori M, Murata T, Iidaka T, Yamada H, Okada T, et al. Differential amygdala response during facial recognition in patients with schizophrenia: an fMRI study. Schizophr Res. 2002;57(1):87–95. https://doi.org/10.1016/S0920-9964(01)00324-3.

  14. Canli T, Cooney RE, Goldin P, Shah M, Sivers H, Thomason ME, et al. Amygdala reactivity to emotional faces predicts improvement in major depression. Neuroreport. 2005;16(12):1267–70. https://doi.org/10.1097/01.wnr.0000174407.09515.cc.

  15. Salgado-Pineda P, Delaveau P, Blin O, Nieoullon A. Dopaminergic contribution to the regulation of emotional perception. Clin Neuropharmacol. 2005;28(5):228–37. https://doi.org/10.1097/01.wnf.0000185824.57690.f0.

    Article  PubMed  CAS  Google Scholar 

  16. Clark US, Neargarder S, Cronin-Golomb A. Specific impairments in the recognition of emotional facial expressions in Parkinson’s disease. Neuropsychologia. 2008;46(9):2300–9. https://doi.org/10.1016/j.neuropsychologia.2008.03.014.

    Article  PubMed  PubMed Central  Google Scholar 

  17. Bediou B, Franck N, Saoud M, Baudouin JY, Tiberghien G, Dalery J, et al. Effects of emotion and identity on facial affect processing in schizophrenia. Psychiatry Res. 2005;133(2-3):149–57. https://doi.org/10.1016/j.psychres.2004.08.008.

    Article  PubMed  Google Scholar 

  18. Bediou B, Asri F, Brunelin J, Krolak-Salmon P, D’amato T, Saoud M, et al. Emotion recognition and genetic vulnerability to schizophrenia. Br J Psychiatry. 2007;191(02):126–30. https://doi.org/10.1192/bjp.bp.106.028829.

    Article  PubMed  Google Scholar 

  19. Schmahmann JD, Sherman JC. The cerebellar cognitive affective syndrome. Brain. 1998;121(4):561–79. https://doi.org/10.1093/brain/121.4.561.

    Article  PubMed  Google Scholar 

  20. Marien P, de Smet HJ, Wijgerde E. Posterior fossa syndrome in adults: a new case and comprehensive survey of the literature. Cortex. 2013;49(1):284–300. https://doi.org/10.1016/j.cortex.2011.06.018.

    Article  PubMed  Google Scholar 

  21. Ozimek A, Richter S, Hein-Kropp C. Cerebellar mutism––report of four cases. J Neurol. 2004;251(8):963–72. https://doi.org/10.1007/s00415-004-0472-6.

    Article  PubMed  CAS  Google Scholar 

  22. Fusar-Poli P, Placentino A, Carletti F. Functional atlas of emotional faces processing: a voxel-based meta-analysis of 105 functional magnetic resonance imaging studies. J Psychiatry Neurosci. 2009;34(6):418–32.

    PubMed  PubMed Central  Google Scholar 

  23. Ferrucci R, Giannicola G, Rosa M. Cerebellum and processing of negative facial emotions: cerebellar transcranial DC stimulation specifically enhances the emotional recognition of facial anger and sadness. Cognit Emot. 2012;26(5):786–99. https://doi.org/10.1080/02699931.2011.619520.

    Article  Google Scholar 

  24. Adamaszek M, D'Agata F, Kirkby KC. Impairment of emotional facial expression and prosody discrimination due to ischemic cerebellar lesions. Cerebellum. 2014;13(3):338–45. https://doi.org/10.1007/s12311-013-0537-0.

    Article  PubMed  CAS  Google Scholar 

  25. Nieto A, Correia R, de Nóbrega E, Montón F, Hess S, Barroso J. Cognition in Friedreich’s ataxia. Cerebellum. 2012;11(4):834–44. https://doi.org/10.1007/s12311-012-0363-9.

    Article  PubMed  Google Scholar 

  26. Reetz K, Dogan I, Costa AS, Dafotakis M, Fedosov K, Giunti P, et al. Biological and clinical characteristics of the European Friedreich’s ataxia consortium for translational studies (EFACTS) cohort: a cross-sectional analysis of baseline data. Lancet Neurol. 2015;14(2):174–82. https://doi.org/10.1016/S1474-4422(14)70321-7.

  27. da Silva CB, Chevis CF, D’Abreu A, Lopes-Cendes I, Franca MC Jr. Fatigue is frequent and multifactorial in Friedreich’s ataxia. Parkinsonism Relat Disord. 2013;19(8):766–7. https://doi.org/10.1016/j.parkreldis.2013.04.007.

    Article  PubMed  Google Scholar 

  28. Nieto A, Hernandez-Torrez A, Perez-Flores J, Monton F. Depressive symptoms in Friedreich ataxia. Int J Clin Health Psychol. 2017;18:18–26.

    Article  PubMed  PubMed Central  Google Scholar 

  29. White M, Lalonde R, Botez-Marquard T. Neuropsychologic and neuropsychiatric characteristics of patients with Freidreich’s ataxia. Acta Neurol Scand. 2000;102(4):222–6. https://doi.org/10.1034/j.1600-0404.2000.102004222.x.

    Article  PubMed  CAS  Google Scholar 

  30. Mantovan M, Martinuzzi A, Squarzanti F, Bolla A, Silvestri I, Liessi G. Exploring mental status in Friedreich’s ataxia: a combined neuropsychological, behavioral and neuroimaging study. Eur J Neurol. 2006;13(8):827–35. https://doi.org/10.1111/j.1468-1331.2006.01363.x.

    Article  PubMed  CAS  Google Scholar 

  31. Dogan I, Tinneman E, Romanzetti S, Mirzazade S, Costa AS, Werner CJ, et al. Cognition in Friedreich’s ataxia: a behavioral and multimodal imaging study. Ann Clin Transl Neurol. 2016;3(8):572–87. https://doi.org/10.1002/acn3.315.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Corben LA, Delatycki MB, Bradshaw JL. Impairment in motor reprogramming in Friedreich ataxia reflecting possible cerebellar dysfunction. J Neurol. 2010;257(5):782–91. https://doi.org/10.1007/s00415-009-5410-1.

    Article  PubMed  Google Scholar 

  33. Hoche F, Guell X, Sherman JC, Vangel MG, Schmahmann JD. Cerebellar contribution to social cognition. 2016;15:732–43.

  34. Campuzano V, Montermini L, Moltò MD, Pianese L, Cossée M. Friedreich’s ataxia: autosomal recessive disease caused by an intronic GAA triplet repeat expansion. Science. 1996;271(5254):1423–7. https://doi.org/10.1126/science.271.5254.1423.

    Article  PubMed  CAS  Google Scholar 

  35. Saccà F, Marsili A, Puorro G, Antenora A, Pane C, Tessa A, et al. Clinical use of frataxin measurement in a patient with a novel deletion in the FXN gene. J Neurol. 2013;260(4):1116–21. https://doi.org/10.1007/s00415-012-6770-5.

  36. Saccà F, Costabile T, Abate F, Liguori A, Paciello F, Pane C, et al. Normalization of timed neuropsychological tests with the use of the PATA rate and nine-hole pegboard tests. J Neuropsychol. 2017. https://doi.org/10.1111/jnp.12125.

  37. Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, et al. The Montreal cognitive assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc. 2005;53(4):695–9. https://doi.org/10.1111/j.1532-5415.2005.53221.x.

    Article  PubMed  Google Scholar 

  38. Orsini A, Grossi D, Capitani E, Laiacona M, Papagno C, Vallar G. Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. It J Neurol Sci. 1987;8(6):537–48. https://doi.org/10.1007/BF02333660.

    Article  Google Scholar 

  39. Rao SM. The cognitive function study Group of the National Multiple Sclerosis Society. A manual for the brief repeatable battery of neuropsychology tests in multiple sclerosis. Medical College of Wisconsin: Milwaukee; 1990.

    Google Scholar 

  40. Carlesimo GA, Buccione I, Fadda L, Graceffa A, Mauri M, Lorusso S, et al. Standardizzazione di due test di memoria per uso clinico. Breve racconto e figura di Rey. Nuova Riv Neurol. 2002;12:1–13.

    Google Scholar 

  41. Giovagnoli AR, Del Pesce M, Mascheroni S, Simoncelli M, Laiacona M, Capitani E. Trail making test: normative values from 287 normal adult controls. Ital J Neurol Sci. 1996;17(4):305–9. https://doi.org/10.1007/BF01997792.

    Article  PubMed  CAS  Google Scholar 

  42. Caffarra P, Vezzadini G, Dieci F, Zonato A, Venneri A. Una versione abbreviata del test di Stroop: dati normativi nella popolazione italiana. Nuova Riv Neurol. 2002;12:111–5.

    Google Scholar 

  43. Novelli G, Papagno C, Capitani E, Laiacona M, Cappa SF, Vallar G. Tre test clinici di ricerca e produzione lessicale. Taratura su soggetti normali. Arch Psicol Neurol Psichiatr. 1996;47:477–506.

    Google Scholar 

  44. Della Sala S, Muggia S, Spinnler H, Zuffi M. Un test di decisione fisionomica tarato su normali ed utilizzato nei dementi di Alzheimer. Arch Psicol Neurol Psichiatr. 1995;56:613–25.

    Google Scholar 

  45. Spitzer RL, Kroenke K, Williams JBW. Validation and utility of a self-report version of PRIME-MD—the PHQ primary care study. JAMA. 1999;282(18):1737–44. https://doi.org/10.1001/jama.282.18.1737.

    Article  PubMed  CAS  Google Scholar 

  46. Spitzer RL, Williams JBW, Kroenke K, Hornyak R, McMurray J. Validity and utility of the PRIME-MD patient health questionnaire in assessment of 3000 obstetric-gynecologic patients: the PRIME- MD patient health questionnaire obstetrics gynecology study. Am J Obstet Gynecol. 2000;183(3):759–69. https://doi.org/10.1067/mob.2000.106580.

    Article  PubMed  CAS  Google Scholar 

  47. Spielberger CD, Reheiser EC. Measuring anxiety, anger, depression, and curiosity as emotional states and personality traits with the STAI, STAXI, and STPI. In: Hersen M, Segal DL, Hilsenroth M, editors. Comprehensive handbook of psychological assessment (Vol. 2): personality assessment. New York: Wiley; 2004. p. 74–80.

    Google Scholar 

  48. First MB, Gibbon M, Spitzer RL, Williams JBW, Benjamin LS. Structured clinical interview for DSM-IV Axis II personality disorders, (SCID-II). Washington, D.C.: American Psychiatric Press, Inc.; 1997.

    Google Scholar 

  49. Bänziger T, Scherer KR, Hall JA, Rosenthal R. Introducing the MiniPONS: a short multichannel version of the profile of nonverbal sensitivity (PONS). J Nonverbal Behav. 2011;35(3):189–204. https://doi.org/10.1007/s10919-011-0108-3.

    Article  Google Scholar 

  50. Schlegel K, Grandjean D, Scherer KR. Emotion recognition: unidimensional ability or a set of modality and emotion specific skills? Personal Individ Differ. 2012;53:6–21.

    Article  Google Scholar 

  51. Schlegel K, Grandjean D, Scherer KR. Introducing the Geneva Emotion Recognition Test: an example of Rasch-based test development. Psychol Assess. 2014;26(2):666–72. https://doi.org/10.1037/a0035246.

    Article  PubMed  Google Scholar 

  52. Schmitz-Hübsch T, Giunti P, Stephenson DA, Globas C, Baliko L, Saccà F, et al. SCA functional index: a useful compound performance measure for spinocerebellar ataxia. Neurology. 2008;71(7):486–92. https://doi.org/10.1212/01.wnl.0000324863.76290.19.

    Article  PubMed  Google Scholar 

  53. Bürk K, Mälzig U, Wolf S, Heck S, Dimitriadis K, Schmitz-Hübsch T, et al. Comparison of three clinical rating scales in Friedreich ataxia (FRDA). Mov Disord. 2009;24(12):1779–84. https://doi.org/10.1002/mds.22660.

  54. Saccà F, Puorro G, Marsili A, Antenora A, Pane C, Casali C, et al. Long-term effect of epoetin alfa on clinical and biochemical markers in friedreich ataxia. Mov Disord. 2016;31(5):734–41. https://doi.org/10.1002/mds.26552.

  55. 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.

  56. Harding IH, Corben LA, Storey E, Egan GF, Stagnitti MR, Poudel GR, et al. Fronto-cerebellar dysfunction and dysconnectivity underlying cognition in Friedreich ataxia: the IMAGE-FRDA study. Hum Brain Mapp. 2016;37(1):338–50. https://doi.org/10.1002/hbm.23034.

  57. Schmahmann JD. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. J Neuropsychiatr Clin Neurosci. 2004;16(3):367–78. https://doi.org/10.1176/jnp.16.3.367.

    Article  Google Scholar 

  58. 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 

  59. Parvizi J, Anderson SW, Martin CO, Damasio H, Damasio AR. Pathological laughter and crying: a link to the cerebellum. Brain. 2001;124(9):1708–19. https://doi.org/10.1093/brain/124.9.1708.

    Article  PubMed  CAS  Google Scholar 

  60. Sacchetti B, Scelfo B, Strata P. Cerebellum and emotional behavior. Neuroscience. 2009;162:756–62.

  61. Frith U. Autism: explaining the enigma. Oxford: Blackwell; 1989.

    Google Scholar 

  62. Deruelle C, Rondan C, Gepner B, Tardif C. Spatial frequency and face processing in children with autism and Asperger syndrome. J Autism Dev Disord. 2004;34(2):199–210. https://doi.org/10.1023/B:JADD.0000022610.09668.4c.

    Article  PubMed  Google Scholar 

  63. Koeppen AH, Becker AB, Qian J, Feustel PJ. Friedreich ataxia: hypoplasia of spinal cord and dorsal root ganglia. J Neuropathol Exp Neurol. 2017;76:101–8.

    Article  PubMed  Google Scholar 

  64. Mascalchi M. The cerebellum looks normal in Friedreich ataxia. Am J Neuroradiol. 2013;34(2):E22. https://doi.org/10.3174/ajnr.A3480.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  65. Surcinelli P, Codispoti M, Montebarocci O, Rossi N, Baldaro B. Facial emotion recognition in trait anxiety. J Anxiety Disord. 2006;20(1):110–7. https://doi.org/10.1016/j.janxdis.2004.11.010.

    Article  PubMed  Google Scholar 

  66. Montagne B, Schutters S, Westenberg HG, van Honk J, Kessels RP, de Haan EH. Reduced sensitivity in the recognition of anger and disgust in social anxiety disorder. Cogn Neuropsychiatry. 2006;11(4):389–401. https://doi.org/10.1080/13546800444000254.

    Article  PubMed  Google Scholar 

Download references

Funding

This study did not receive any financial support.

Author information

Authors and Affiliations

  1. Department of Neurosciences and Reproductive and Odontostomatological Sciences, University “Federico II”, Via Pansini, 5, 80131, Naples, NA, Italy

    Teresa Costabile, Veronica Capretti, Filomena Abate, Agnese Liguori, Francesca Paciello, Chiara Pane, Anna De Rosa, Silvio Peluso, Giuseppe De Michele, Alessandro Filla & Francesco Saccà

Authors
  1. Teresa Costabile
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Veronica Capretti
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Filomena Abate
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Agnese Liguori
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Francesca Paciello
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chiara Pane
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Anna De Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Silvio Peluso
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Giuseppe De Michele
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Alessandro Filla
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Francesco Saccà
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

A. Design and conceptualization of the study.

B. Analysis or interpretation of the data.

C. Drafting or revising the manuscript for intellectual content.

Teresa Costabile ABC, Veronica Capretti B, Filomena Abate B, Agnese Liguori B, Francesca Paciello B, Chiara Pane AB, Anna De Rosa AB, Silvio Peluso C, Giuseppe De Michele C, Alessandro Filla C, Francesco Saccà ABC.

Corresponding author

Correspondence to Francesco Saccà.

Ethics declarations

Authors’ Disclosures

All authors have nothing to disclose.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Costabile, T., Capretti, V., Abate, F. et al. Emotion Recognition and Psychological Comorbidity in Friedreich’s Ataxia. Cerebellum 17, 336–345 (2018). https://doi.org/10.1007/s12311-018-0918-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12311-018-0918-5

Keywords

Search

Navigation