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Pathological laughing and crying in amyotrophic lateral sclerosis is related to frontal cortex function

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Abstract

The syndrome of pathological laughing and crying (PLC) is characterized by episodes of involuntary outbursts of emotional expression. Although this phenomenon has been referred to for over a century, a clear-cut clinical definition is still lacking, and underlying pathophysiological mechanisms are not well understood. In particular, it remains ill-defined which kind of stimuli—contextually appropriate or inappropriate—elicit episodes of PLC, and if the phenomenon is a result of a lack of inhibition from the frontal cortex (“top-down-theory”) or due to an altered processing of sensory inputs at the brainstem level (“bottom-up-theory”). To address these questions, we studied ten amyotrophic lateral sclerosis (ALS) patients with PLC and ten controls matched for age, sex and education. Subjects were simultaneously exposed to either emotionally congruent or incongruent visual and auditory stimuli and were asked to rate pictures according to their emotional quality. Changes in physiological parameters (heart rate, galvanic skin response, activity of facial muscles) were recorded, and a standardized self-assessment lability score (CNS-LS) was determined. Patients were influenced in their rating behaviour in a negative direction by mood-incongruent music. Compared to controls, they were influenced by negative stimuli, i.e. they rated neutral pictures more negatively when listening to sad music. Patients rated significantly higher on the CNS-LS. In patients, changes of electromyographic activity of mimic muscles during different emotion-eliciting conditions were explained by frontal cortex dysfunction. We conclude that PLC is associated with altered emotional suggestibility and that it is preferentially elicited by mood-incongruent stimuli. In addition, physiological reactions as well as behavioural changes suggest that this phenomenon is primarily an expression of reduced inhibitory activity of the frontal cortex, since frontal dysfunction could explain changes in physiological parameters in the patient group. We consider these findings being important for the clinical interpretation of emotional reactions of ALS patients.

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References

  1. Abrahams S, Newton J, Niven E, Foley J, Bak TH (2014) Screening for cognition and behaviour changes in ALS. Amyotroph Lateral Scler Frontotemporal Degener 15(1–2):9–14. doi:10.3109/21678421.2013.805784

    Article  PubMed  Google Scholar 

  2. Bradley MM, Greenwald MK, Hamm AO (1993) Affective picture processing. In: Birbaumer N, Öhman A (eds) The structure of emotion. Hogrefe and Huber (publ.)

  3. Brettschneider J, Del Tredici K, Toledo JB, Robinson JL, Irwin DJ, Grossman M, Trojanowski JQ (2013) Stages of pTDP-43 pathology in amyotrophic lateral sclerosis. Ann Neurol 74(1):20–38. doi:10.1002/ana.23937

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Brooks BR, Miller RG, Swash M, Munsat TL, World Federation of Neurology Research Group on Motor Neuron, Diseases (2000) El Escorial revisited: revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotroph Lateral Scler Other Motor Neuron Disord 1(5):293–299

    Article  CAS  PubMed  Google Scholar 

  5. Dark FL, McGrath JJ, Ron MA (1996) Pathological laughing and crying. Aust N Z J Psychiatry 30(4):472–479

    Article  CAS  PubMed  Google Scholar 

  6. Floeter MK, Katipally R, Kim MP, Schanz O, Stephen M, Danielian L, Meoded A (2014) Impaired corticopontocerebellar tracts underlie pseudobulbar affect in motor neuron disorders. Neurology 83(7):620–627. doi:10.1212/WNL.0000000000000693

    Article  PubMed  PubMed Central  Google Scholar 

  7. Gallagher JP (1989) Pathologic laughter and crying in ALS: a search for their origin. Acta Neurol Scand 80(2):114–117

    Article  CAS  PubMed  Google Scholar 

  8. Hartje W (2005) Störungen des emotionalen Verhaltens. In: Karnath HO, Hartje W, Ziegler W (eds) Kognitive Neurologie. Thieme, Stuttgart

    Google Scholar 

  9. Ironside R (1956) Disorders of laughter due to brain lesions. Brain 79(4):589–609

    Article  CAS  PubMed  Google Scholar 

  10. Lang PJ, Greenwald MK, Bradley MM, Hamm AO (1993) Looking at pictures: affective, facial, visceral, and behavioral reactions. Psychophysiology 30(3):261–273

    Article  CAS  PubMed  Google Scholar 

  11. Lang PJ, Bradley MM, Cuthbert BN (2008) International affective picture system (IAPS): affective ratings of pictures and instruction manual. Technical Report A-8. University of Florida, Gainesville

  12. Lule D, Burkhardt C, Abdulla S, Bohm S, Kollewe K, Uttner I, Ludolph AC (2014) The Edinburgh cognitive and behavioural amyotrophic lateral sclerosis screen: a cross-sectional comparison of established screening tools in a German-Swiss population. Amyotroph Lateral Scler Frontotemporal Degener. doi:10.3109/21678421.2014.959451

    Google Scholar 

  13. Lule D, Kurt A, Jurgens R, Kassubek J, Diekmann V, Kraft E, Anders S (2005) Emotional responding in amyotrophic lateral sclerosis. J Neurol 252(12):1517–1524. doi:10.1007/s00415-005-0907-8

    Article  PubMed  Google Scholar 

  14. McCullagh S, Moore M, Gawel M, Feinstein A (1999) Pathological laughing and crying in amyotrophic lateral sclerosis: an association with prefrontal cognitive dysfunction. J Neurol Sci 169(1–2):43–48

    Article  CAS  PubMed  Google Scholar 

  15. Miller A, Pratt H, Schiffer RB (2011) Pseudobulbar affect: the spectrum of clinical presentations, etiologies and treatments. Expert Rev Neurother 11(7):1077–1088. doi:10.1586/ern.11.68

    Article  PubMed  Google Scholar 

  16. Mitterschiffthaler MT, Fu CH, Dalton JA, Andrew CM, Williams SC (2007) A functional MRI study of happy and sad affective states induced by classical music. Hum Brain Mapp 28(11):1150–1162. doi:10.1002/hbm.20337

    Article  PubMed  Google Scholar 

  17. Morris JC, Mohs RC, Rogers H, Fillenbaum G, Heyman A (1988) Consortium to establish a registry for Alzheimer’s disease (CERAD) clinical and neuropsychological assessment of Alzheimer’s disease. Psychopharmacol Bull 24(4):641–652

    CAS  PubMed  Google Scholar 

  18. Murai T, Barthel H, Berrouschot J, Sorger D, von Cramon DY, Muller U (2003) Neuroimaging of serotonin transporters in post-stroke pathological crying. Psychiatry Res 123(3):207–211

    Article  CAS  PubMed  Google Scholar 

  19. Olney NT, Goodkind MS, Lomen-Hoerth C, Whalen PK, Williamson CA, Holley DE, Rosen HJ (2011) Behaviour, physiology and experience of pathological laughing and crying in amyotrophic lateral sclerosis. Brain 134(Pt 12):3458–3469. doi:10.1093/brain/awr297

    Article  PubMed  Google Scholar 

  20. Oppenheim H, Siemerling E (1886) Mitteilungen uber Pseudobulbarparalyse und akute Bulbarparalyse. Berl kli Woch, 46

  21. Parvizi J, Anderson SW, Martin CO, Damasio H, Damasio AR (2001) Pathological laughter and crying: a link to the cerebellum. Brain 124(Pt 9):1708–1719

    Article  CAS  PubMed  Google Scholar 

  22. Parvizi J, Coburn KL, Shillcutt SD, Coffey CE, Lauterbach EC, Mendez MF (2009) Neuroanatomy of pathological laughing and crying: a report of the American Neuropsychiatric Association Committee on Research. J Neuropsychiatry Clin Neurosci 21(1):75–87. doi:10.1176/appi.neuropsych.21.1.75

    Article  PubMed  Google Scholar 

  23. Poeck K (1969) Pathological laughing and weeping in patients with progressive balbar palsy. Ger Med Mon 14(8):394–397

    CAS  PubMed  Google Scholar 

  24. Pollack IF, Polinko P, Albright AL, Towbin R, Fitz C (1995) Mutism and pseudobulbar symptoms after resection of posterior fossa tumors in children: incidence and pathophysiology. Neurosurgery 37(5):885–893

    Article  CAS  PubMed  Google Scholar 

  25. Schandry R (1981) Psychophysiology: Körperliche Indikatoren menschlichen Verhaltens. US Psychologie, Urban und Schwarzenberg, Munchen Wien Baltimore

  26. Schiffer R, Pope LE (2005) Review of pseudobulbar affect including a novel and potential therapy. J Neuropsychiatry Clin Neurosci 17(4):447–454. doi:10.1176/appi.neuropsych.17.4.447

    Article  CAS  PubMed  Google Scholar 

  27. Schwartz GE, Fair PL, Salt P, Mandel MR, Klerman GL (1976) Facial muscle patterning to affective imagery in depressed and nondepressed subjects. Science 192(4238):489–491

    Article  CAS  PubMed  Google Scholar 

  28. Smith RA, Berg JE, Pope LE, Thisted RA (2004) Measuring pseudobulbar affect in ALS. Amyotroph Lateral Scler Other Motor Neuron Disord 5(Suppl 1):99–102. doi:10.1080/17434470410020058

    Article  PubMed  Google Scholar 

  29. Wilson SAK (1924) Some problems in neurology. II: pathological laughing and crying. J Neurol Psychopathol 4:299–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Authors and Affiliations

  1. Department of Neurology, University Hospital of Ulm, Oberer Eselsberg 45, 89081, Ulm, Germany

    Annemarie Hübers, Jan Kassubek, Martin Gorges, Helena Aho-Oezhan, Jürgen Keller, Hannah Horn, Hermann Neugebauer, Ingo Uttner, Dorothée Lulé & Albert C. Ludolph

  2. Department of Psychiatry, University Hospital of Ulm, Leimgrubenweg 12-14, 89073, Ulm, Germany

    Georg Grön

Authors
  1. Annemarie Hübers
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  2. Jan Kassubek
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Correspondence to Annemarie Hübers.

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Appendix 1: List of musical excerpts

Appendix 1: List of musical excerpts

 

Composer

Title

Sad

Albinoni

Adagio in sol minor

Bruch

Kol Nidrei

Grieg

Solveig’s song—Peer Gynt

Rodrigo

Concerto de Aranjuez

Sinding

Suite for violin & orchestra A minor

Happy

Bizet

Chanson du toreador—Carmen

Mozart

Allegro—A little night music

Mozart

Rondo Allegro—A little night music

Strauß

Blue Danube

Strauß

Radetzky march

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Hübers, A., Kassubek, J., Grön, G. et al. Pathological laughing and crying in amyotrophic lateral sclerosis is related to frontal cortex function. J Neurol 263, 1788–1795 (2016). https://doi.org/10.1007/s00415-016-8201-5

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  • DOI: https://doi.org/10.1007/s00415-016-8201-5

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