Skip to main content
SpringerLink
Log in

Brain responses to emotional stimuli in patients with amyotrophic lateral sclerosis (ALS)

  • ORIGINAL COMMUNICATION
  • Published:
Journal of Neurology Aims and scope Submit manuscript

Abstract

Amyotrophic lateral sclerosis (ALS), a progressive motor neuron disease, affects movement and communication abilities and emotional processing. Subjective ratings of emotional stimuli depicting social interactions and facial expressions differed significantly between ALS patients and healthy controls in a previous study with a reduction of negative emotional valence (pleasantness) and lower subjective arousal (excitement) in ALS patients. In the present study, sixty similar emotional slides were presented to 13 ALS patients, 15 matched healthy controls and six tetraplegic patients. Subjective reports of valence and arousal as well as brain responses to the affective pictures using functional magnetic resonance imaging (fMRI) were measured. The picture series was presented twice with a 6-months interval to investigate effects of disease progression. ALS patients presented an increased brain response in the right supramarginal area and a reduced brain response in extrastriate visual areas at both measurements compared with healthy controls. Within the ALS patients' group a reduction of brain responses in the anterior insula at the follow-up was correlated with the subjective arousal. The reduced response in the anterior insula is tentatively interpreted as indicating reduced arousal during the course of the disease at the neural and behavioural level. The reduction of activity in extrastriate visual areas might be similarly interpreted. The increased brain response in the right supramarginal area of ALS patients might represent an altered sensitivity to social-emotional cues.

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

Similar content being viewed by others

References

  1. Adolphs R, Damasio H, Tranel D, Cooper G, Damasio AR (2000) A role for somatosensory cortices in the visual recognition of emotion as revealed by three-dimensional lesion mapping. J Neurosci 20(7):2683–90

    PubMed  CAS  Google Scholar 

  2. Anders S, Lotze M, Erb M, Grodd W, Birbaumer N (2004) Brain activity underlying emotional valence and arousal: A response-related fMRI study. Hum Brain Map 23:200–209

    Article  Google Scholar 

  3. Angevine JB, Cotman CW (1981) The limbic system and hypothalamus. In: Principles of neuroanatomy. Oxford University Press, New York:253–293

  4. Aschenbrenner S, Tucha O, Lange K (2000) Regensburger Wortflüssigkeits- Test. Hogrefe-Verlag, Göttingen

  5. Baddeley A, Emslie H, Nimmo-Smith I (1994) Doors and people: A test of visual and verbal recall and recognition. Thames Valley Test Company Ltd, Bury St Edmunds

    Google Scholar 

  6. Brooks BR (1998) Revised Criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases of World Federation of Neurology Research Group on Neuromuscular Diseases, El Escorial “Clinical Limits of ALS” Workshop Contributors (1994). El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. J Neur Sci 124:96–107; (http://www.wfnals.org/guidelines/1998elescorial/elescorial1998.htm)

    Google Scholar 

  7. Brown WA, Mueller PS (1970) Psychological function in individuals with amyotrophic lateral sclerosis (ALS). Psychosom Med 32(2):141–52

    PubMed  CAS  Google Scholar 

  8. Buccino G, Lui F, Canessa N, Patteri I, Lagravinese G, Benuzzi F, Porro CA, Rizzolatti G (2004) Neural circuits involved in the recognition of actions performed by nonconspecifics: an FMRI study. J Cogn Neurosci 16(1):114–26

    Article  PubMed  Google Scholar 

  9. Cedarbaum JM, Stambler N, Malta E, Fuller C, Hilt D, Thurmond B, Nakanishi A (1999) The ALSFRS-R: a revised ALS functional rating scale that incorporates assessments of respiratory function. BDNF ALS Study Group (Phase III). J Neurol Sci 169(1–2):13–21

    Article  PubMed  CAS  Google Scholar 

  10. Craig AD (2002) How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3(8):655–66

    PubMed  CAS  Google Scholar 

  11. Dale AM (1999) Optimal experimental design for event-related fMRI. Hum Brain Map 8:109–114

    Article  CAS  Google Scholar 

  12. Damasio AR, Tranel D, Damasio H (1991) Somatic markers and the guidance of behaviour: theory and preliminary testing. In: Levin HS, Eisenberg HM, Benton AL, (eds) Frontal Lobe Function and Dysfunction. University Press, New York, Oxford, pp 217–229

  13. Deichmann R, Turner R (2002) Improvement of local BOLD sensitivities in the presence of susceptibility gradients by using tilted slices. Proc of the International Society of Magnetic Resonance in Medicine 10:1414

    Google Scholar 

  14. Folstein MF, Folstein SE, McHugh PR (1975) Mini-Mental-State: A practical method for grading the cognitive state of patients for the clinician. J Psych Res 12:189–198

    Article  CAS  Google Scholar 

  15. Friston KJ, Fletcher P, Josephs O, Holmes A, Rugg MD, Turner R (1998) Event-related fMRI: characterizing differential responses. Neuroimage 7(1):30–40

    Article  PubMed  CAS  Google Scholar 

  16. Friston KJ, Glaser DE, Henson RNA, Kiebel S, Phillips C, Ashburner J (2002) Classical and Bayesian Inference in Neuroimaging: Applications. Neuroimage 16:484–512

    Article  PubMed  CAS  Google Scholar 

  17. Friston KJ, Holmes AP, Worsley KJ, Poline J-P, Frith CD, Frackowiak RSJ (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Map 2:189–210

    Article  Google Scholar 

  18. Grill-Spector K (2003) The neural basis of object perception. Curr Opin Neurobiol 13(2):159–66

    Article  PubMed  CAS  Google Scholar 

  19. Hall DA, Fussell C, Summerfield AQ (2005) Reading fluent speech from talking faces: typical brain networks and individual differences. J Cogn Neurosci 17(6):939–53

    Article  PubMed  Google Scholar 

  20. Hautzinger M, Bailer M, Worall H, Keller F (1995) Beck-Depressions-Inventar, BDI – Testhandbuch, 2nd ed., Verlag Hans Huber, Bern, pp 7–17

  21. Kanwisher N, Wojciulik E (2000) Visual attention: insights from brain imaging. Nat Rev Neurosci 1(2):91–100

    Article  PubMed  CAS  Google Scholar 

  22. Kawashima T, Doh-ura K, Kikuchi H, Iwaki T (2001) Cognitive dysfunction in patients with amyotrophic lateral sclerosis is associated with spherical or crescent-shaped ubiquitinated intraneuronal inclusions in the parahippocampal gyrus and amygdala, but not in the neostriatum. Acta Neuropathol (Berl) 102(5):467–72

    CAS  Google Scholar 

  23. Kew JJM, Goldstein LH, Leigh PN, Abrahams S, Cosgrave N, Passingham RE (1993) The relationship between abnormalities of cognitive function and cerebral activation in amyotrophic lateral sclerosis. Brain 116:1399–1423

    Article  PubMed  Google Scholar 

  24. Kourtzi Z, Kanwisher N (2000) Activation in human MT/MST by static images with implied motion. J Cogn Neurosci 12(1):48–55

    Article  PubMed  CAS  Google Scholar 

  25. Kübler A, Winter S, Kaiser J, Birbaumer N, Hautzinger M (2005) Ein Fragebogen zur Messung von Depression bei degenerativen neurologischen Erkrankungen (amyotrophe Lateralsklerose) - A questionnaire to measure depression in degenerative neurological diseases. Z. Klin. Psychol. Psychother 31(1):19–26

    Article  Google Scholar 

  26. Lang PJ, Bradley MM, Fitzsimmons JR, Cuthbert BN, Scott JD, Moulder B, Nangia V (1998) Emotional arousal and activation of the visual cortex: an fMRI analysis. Psychophysiology 35(2):199–210

    Article  PubMed  CAS  Google Scholar 

  27. Lang PJ, Bradley MM, Cuthbert BN (1999) International affective picture system (IAPS): Technical manual and affective ratings. Center for Reserach in Psychophysiology, University of Florida, Gainsville

  28. Leigh PN, Simmons A, Williams S, Williams V, Turner M, Brooks D (2002) Imaging: MRS/MRI/PET/SPECT: summary. Amyotroph Lateral Scler Other Motor Neuron Disord 3(1):75–80

    Article  Google Scholar 

  29. Lehrl S (1989) Mehrfachwahl-Wortschatz- Intelligenztest MWT-B. Manual, 2nd ed., Perimed Fachbuch-Verlagsgesellschaft, Erlangen

  30. Lewandowski LJ (1984) The symbol digits modalities test: A screening for brain-damaged children. Percept Mot Skills 59(2):615–618

    PubMed  CAS  Google Scholar 

  31. Lulé D, Kurt A, Jurgens R, Kassubek J, Diekmann V, Kraft E, Neumann N, Ludolph AC, Birbaumer N, Anders S (2005) Emotional responding in amyotrophic lateral sclerosis. J Neurol 252:1517–1524

    Article  PubMed  Google Scholar 

  32. Nelson HE (1976) A modified card sorting test sensitive to frontal lobe defects. Cortex 12:313–324

    PubMed  CAS  Google Scholar 

  33. Papps B, Abrahams S, Wicks P, Leigh PN, Goldstein LH (2005) Changes in memory for emotional material in amyotrophic lateral sclerosis (ALS). Neuropsychologia 43(8):1107–14

    Article  PubMed  CAS  Google Scholar 

  34. Peuskens H, Vanrie J, Verfaillie K, Orban GA (2005) Specificity of regions processing biological motion. Eur J Neurosci 21(10):2864–75

    Article  PubMed  CAS  Google Scholar 

  35. Pegna AJ, Khateb A, Lazeyras F, Seghier ML(1984) Discriminating emotional faces without primary visual cortices involves the right amygdala. Nat Neurosci. 8(1):24–5. Epub 2004 Dec 12

    Google Scholar 

  36. Phan KL, Wager T, Taylor SF, Liberzon I (2002) Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 16(2):331–48

    Article  PubMed  Google Scholar 

  37. Regard M, Strauss E, Knapp P (1982) Childrens' production on verbal and non-verbal fluency tasks. Perceptual and Motor Skills 55:839–844

    PubMed  CAS  Google Scholar 

  38. Yoshimura N, Kawamura M, Masaoka Y, Homma I (2005) The amygdala of patients with Parkinson's disease is silent in response to fearful facial expressions. Neuroscience 131(2):523–34

    Article  PubMed  CAS  Google Scholar 

  39. Young A, Perrett D, Calder A, Sprengelmeyer R, Ekman P (2002) Facial Expressions of Emotion: Stimuli and Tests (FEEST), Version for PC. Thames Valley Test Company Thurston, UK

Download references

Author information

Authors and Affiliations

  1. Dept. of Neurophysiology, University of Ulm, Albert-Einstein-Allee 47, 89081, Ulm, Germany

    Dorothée Lulé, Volker Diekmann & Jan Kassubek

  2. Dept. of Neurology, University of Ulm, Germany

    Dorothée Lulé, Volker Diekmann, Jan Kassubek & Albert C. Ludolph

  3. Institute of Medical Psychology and Behavioral Neurobiology, Eberhard-Karls-University Tübingen, Germany

    Dorothée Lulé, Silke Anders, Andrea Kübler & Niels Birbaumer

  4. National Institutes of Health, NINDS Human Cortical Physiology, Bethesda, US

    Niels Birbaumer

Authors
  1. Dorothée Lulé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Volker Diekmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Silke Anders
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jan Kassubek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea Kübler
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Albert C. Ludolph
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Niels Birbaumer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dorothée Lulé.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lulé, D., Diekmann, V., Anders, S. et al. Brain responses to emotional stimuli in patients with amyotrophic lateral sclerosis (ALS). J Neurol 254, 519–527 (2007). https://doi.org/10.1007/s00415-006-0409-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00415-006-0409-3

Key words

Search

Navigation