The brain correlates of laugh and cataplexy in childhood narcolepsy

Journal of Neuroscience

Volumn 35, Issue 33, 2015, Pages 11583-11594

  Meletti, Stefano ^a,b   Vaudano, Anna Elisabetta ^a,b   Pizza, Fabio ^c,d   Ruggieri, Andrea ^a   Vandi, Stefano ^c,d   Teggi, Alberto ^a   Franceschini, Christian ^e   Benuzzi, Francesca ^a   Nichelli, Paolo Frigio ^a,b   Plazzi, Giuseppe ^c,d  

^a UNIVERSITY OF MODENA AND REGGIO EMILIA   (Italy)

^b AUSL Modena   (Italy)

^c UNIVERSITY OF BOLOGNA   (Italy)

^d IRCCS ISTITUTO DELLE SCIENZE NEUROLOGICHE DI BOLOGNA   (Italy)

^e UNIVERSITY OF PARMA   (Italy)

Author keywords

Cataplexy; Emotion; fMRI; Humor; Narcolepsy; Sleep disorders

Indexed keywords

ADOLESCENT; ANTERIOR CINGULATE; ANTERIOR INSULAR CORTEX; ANTEROMEDIAL PONS; ARTICLE; BOLD SIGNAL; BRAIN REGION; CATAPLEXY; CHILD; CLINICAL ARTICLE; ELECTROENCEPHALOGRAPHY; FACIAL EXPRESSION; FEMALE; FRONTAL OPERCULUM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; LAUGHTER; LOCUS CERULEUS; MALE; MUSCLE CONTRACTION; MUSCLE HYPOTONIA; MUSCLE TONE; NARCOLEPSY; NUCLEUS ACCUMBENS; POLYSOMNOGRAPHY; PREMOTOR CORTEX; PRIORITY JOURNAL; PTOSIS; SCHOOL CHILD; VENTROMEDIAL PREFRONTAL CORTEX; BRAIN; BRAIN MAPPING; FACE MUSCLE; NERVE CELL NETWORK; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; STATISTICS;

BRAIN; BRAIN MAPPING; CATAPLEXY; CHILD; FACIAL MUSCLES; FEMALE; HUMANS; LAUGHTER; MAGNETIC RESONANCE IMAGING; MALE; NARCOLEPSY; NERVE NET; STATISTICS AS TOPIC;

EID: 84939817312     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0840-15.2015     Document Type: Article

References (56)

1. American Academy of Sleep Medicine (2014) International classification of sleep disorders, ed 3. Darien, IL: American Academy of Sleep Medicine.
2. Avanzini P, Vaudano AE, Vignoli A, Ruggieri A, Benuzzi F, Darra F, Mastrangelo M, Dalla Bernardina B, Nichelli PF, Canevini MP, Meletti S (2014) Low frequency mu-like activity characterizes cortical rhythms in epilepsy due to ring chromosome 20. Clin Neurophysiol 125:239 -249. CrossRef Medline
3. Bartolo A, Benuzzi F, Nocetti L, Baraldi P, Nichelli P (2006) Humor comprehension and appreciation: an FMRI study. J Cogn Neurosci 18:1789- 1798. CrossRef Medline
4. Blouin AM, Fried I, Wilson CL, Staba RJ, Behnke EJ, Lam HA, Maidment NT, Karlsson KÆ, Lapierre JL, Siegel JM (2013) Human hypocretin and melanin-concentrating hormone levels are linked to emotion and social interaction. Nat Commun 4:1547. CrossRef Medline
5. Burgess CR, Scammell TE (2012) Narcolepsy: neural mechanisms of sleepiness and cataplexy. J Neurosci 32:12305-12311. CrossRef Medline
6. Burgess CR, Oishi Y, Mochizuki T, Peever JH, Scammell TE (2013) Amygdala lesions reduce cataplexy in orexin knock-out mice. J Neurosci 33:9734 -9742. CrossRef Medline
7. Chabas D, Habert MO, Maksud P, Tourbah A, Minz M, Willer JC, Arnulf, I (2007) Functional imaging of cataplexy during status cataplecticus. Sleep 30:153-156. Medline
8. Chaudhary UJ, Rodionov R, Carmichael DW, Thornton RC, Duncan JS, Lemieux L (2012) Improving the sensitivity of EEG-fMRI studies of epileptic activity by modelling eye blinks, swallowing and other video-EEG detected physiological confounds. Neuroimage 61:1383-1393. CrossRef Medline
9. Cle´ment O, Sapin E, Libourel PA, Arthaud S, Brischoux F, Fort P, Luppi PH (2012) The lateral hypothalamic area controls paradoxical (REM) sleep by means of descending projections to brainstem GABAergic neurons. J Neurosci 32:16763-16774. CrossRef Medline
10. Craig AD (2009) How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10:59 -70. CrossRef Medline
11. Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J, Hichwa RD (2000) Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3:1049 -1056. CrossRef Medline
12. Dauvilliers Y, Arnulf I, Mignot E (2007) Narcolepsy with cataplexy. Lancet 369:499 -511. CrossRef Medline
13. Dauvilliers Y, Comte F, Bayard S, Carlander B, Zanca M, Touchon J (2010) A brain PET study in patients with narcolepsy-cataplexy. J Neurol Neurosurg Psychiatry 81:344 -348. CrossRef Medline
14. Dauvilliers Y, Siegel JM, Lopez R, Torontali ZA, Peever JH (2014) Cataplexy- clinical aspects, pathophysiology and management strategy. Nat Rev Neurol 10:386 -395. CrossRef Medline
15. Friston KJ, Williams S, Howard R, Frackowiak RS, Turner R (1996) Movement-related effects in fMRI time-series. Magn Reson Med 35:346- 355. CrossRef Medline
16. Friston KJ, Holmes AP, Price CJ, Bu¨chel C, Worsley KJ (1999) Multisubject fMRI studies and conjunction analyses. Neuroimage 10:385-396. CrossRef Medline
17. Goel V, Dolan RJ (2001) The functional anatomy of humor: segregating cognitive and affective components. Nat Neurosci 4:237-238. CrossRef Medline
18. Gulyani S, Wu MF, Nienhuis R, John J, Siegel JM (2002) Cataplexy-related neurons in the amygdala of the narcoleptic dog. Neuroscience 112:355- 365. CrossRef Medline
19. Hong SB, Tae WS, Joo EY (2006) Cerebral perfusion changes during cataplexy in narcolepsy patients. Neurology 66:1747-1749. CrossRef Medline
20. Kaur S, Thankachan S, Begum S, Liu M, Blanco-Centurion C, Shiromani PJ (2009) Hypocretin-2 saporin lesions of the ventrolateral periaqueductal gray (vlPAG) increase REM sleep in hypocretin knock-out mice. PLoS One 4:e6346. CrossRef Medline
21. Khatami R, Birkmann S, Bassetti CL (2007) Amygdala dysfunction in narcolepsy-cataplexy. J Sleep Res 16:226 -229. CrossRef Medline
22. Knutson B, FongGW,Bennett SM, Adams CM,HommerD (2003) Aregion of medial prefrontal cortex tracks monetarily rewarding outcomes: characterization with rapid event-related fMRI. Neuroimage 18:263-272. CrossRef Medline
23. Littner MR, Kushida C, Wise M, Davila DG, Morgenthaler T, Lee-Chiong T, Hirshkowitz M, Daniel LL, Bailey D, Berry RB, Kapen S, Kramer M, Kramer M (2005) Standards of Practice Committee of the American Academy of Sleep Medicine. Practice parameters for clinical use of the multiple sleep latency test and the maintenance of wakefulness test. Sleep 28:113-121. Medline
24. Longstreth WT Jr, Koepsell TD, Ton TG, Hendrickson AF, van Belle G (2007) The epidemiology of narcolepsy. Sleep 30:13-26. Medline
25. Melendres MC, Lutz JM, Rubin ED, Marcus CL (2004) Daytime sleepiness and hyperactivity in children with suspected sleep-disordered breathing. Pediatrics 114:768 -775. CrossRef Medline
26. Mileykovskiy BY, Kiyashchenko LI, Siegel JM (2005) Behavioral correlates of activity in identified hypocretin/orexin neurons. Neuron 46:787-798. CrossRef Medline
27. Mobbs D, Greicius MD, Abdel-Azim E, Menon V, Reiss AL (2003) Humor modulates the mesolimbic reward centers. Neuron 40:1041-1048. CrossRef Medline
28. Moran JM, Wig GS, Adams RB Jr, Janata P, KelleyWM (2004) Neural correlates of humor detection and appreciation. Neuroimage 21:1055-1060. CrossRef Medline
29. Oishi Y, Williams RH, Agostinelli L, Arrigoni E, Fuller PM, Mochizuki T, Saper CB, Scammell TE (2013) Role of the medial prefrontal cortex in cataplexy. J Neurosci 33:9743-9751. CrossRef Medline
30. Oldfield RC (1971) The Assessment and analysis of handedness: the Edinburgh Inventory. Neuropsychologia 9:97-113. CrossRef Medline
31. Overeem S, Lammers GJ, van Dijk JG (1999) Weak with laughter. Lancet 354:838. CrossRef Medline
32. Overeem S, van Nues SJ, van der Zande WL, Donjacour CE, van Mierlo P, Lammers GJ (2011) The clinical features of cataplexy: a questionnaire study in narcolepsy patients with and without hypocretin-1 deficiency. Sleep Med 12:12-18. CrossRef Medline
33. Partinen M, Kornum BR, Plazzi G, Jennum P, Julkunen I, Vaarala O (2014) Narcolepsy as an autoimmune disease: the role of H1N1 infection and vaccination. Lancet Neurol 13:600-613. CrossRef Medline
34. Peyron C, Faraco J, Rogers W, Ripley B, Overeem S, Charnay Y,Nevsimalova S, Aldrich M, Reynolds D, Albin R, Li R, Hungs M, Pedrazzoli M, Padigaru M, Kucherlapati M, Fan J, Maki R, Lammers GJ, Bouras C, Kucherlapati R, et al. (2000) A mutation in case of early onset narcolepsy and a generalized absence of hypocretin peptides in human narcoleptic brains. Nat Med 6:991-997. CrossRef Medline
35. Pizza F, Franceschini C, Peltola H, Vandi S, Finotti E, Ingravallo F, Nobili L, Bruni O, Lin L, Edwards MJ, Partinen M, Dauvilliers Y, Mignot E, Bhatia KP, PlazziG (2013) Clinical and polysomnographic course of childhood narcolepsy with cataplexy. Brain 136:3787-3795. CrossRef Medline
36. Pizza F, Peltola H, Sarkanen T, Moghadam KK, Plazzi G, PartinenM (2014) Childhood narcolepsy with cataplexy: comparison between post-H1N1 vaccination and sporadic cases. Sleep Med 15:262-265. CrossRef Medline
37. Plazzi G, Pizza F (2013) Childhood narcolepsy with cataplexy: a newly reported phenotype of an old disease? Sleep Med 14:810-811. CrossRef Medline
38. Plazzi G, Pizza F, Palaia V, Franceschini C, Poli F, Moghadam KK, Cortelli P, Nobili L, Bruni O, Dauvilliers Y, Lin L, Edwards MJ, Mignot E, Bhatia KP (2011) Complex movement disorders at disease onset in childhood narcolepsy with cataplexy. Brain 134:3477-3489. CrossRef Medline
39. Ponz A, Khatami R, Poryazova R, Werth E, Boesiger P, Bassetti CL, Schwartz S (2010a) Abnormal activity in reward brain circuits in human narcolepsy with cataplexy. Ann Neurol 67:190 -200. CrossRef Medline
40. Ponz A, Khatami R, Poryazova R, Werth E, Boesiger P, Schwartz S, Bassetti CL (2010b) Reduced amygdala activity during aversive conditioning in human narcolepsy. Ann Neurol 67:394 -398. CrossRef Medline
41. Reiss AL, Hoeft F, Tenforde AS, Chen W, Mobbs D, Mignot EJ (2008) Anomalous hypothalamic responses to humor in cataplexy. PLoS One 3:e2225. CrossRef Medline
42. Rubboli G, d'Orsi G, Zaniboni A, Gardella E, Zamagni M, Rizzi R, Meletti S, Valzania F, Tropeani A, Tassinari CA (2000) A video-polygraphic analysis of the cataplectic attack. Clin Neurophysiol 111 [Suppl 2]:S120 -S128. CrossRef Medline
43. Ruggieri A, Vaudano AE, Benuzzi F, Serafini M, Gessaroli G, Farinelli V, Nichelli PF, Meletti S (2015) Mapping (and modeling) physiological movements during EEG-fMRI recordings: the added value of the VIDEO acquired simultaneously. J Neurosci Methods 239:223-237. CrossRef Medline
44. Sabatinelli D, Bradley MM, Lang PJ, Costa VD, Versace F (2007) Pleasure rather than salience activates human nucleus accumbens and medial prefrontal cortex. J Neurophysiol 98:1374 -1379. CrossRef Medline
45. Schenck CH, Bassetti CL, Arnulf I, Mignot E (2007) English translations of the first clinical reports on narcolepsy and cataplexy by Westphal and Ge´lineau in the late 19th century, with commentary. J Clin Sleep Med 3:301-311. Medline
46. Schwartz S, Ponz A, Poryazova R, Werth E, Boesiger P, Khatami R, Bassetti CL (2008) Abnormal activity in hypothalamus and amygdala during humour processing in human narcolepsy with cataplexy. Brain 131:514- 522. CrossRef Medline
47. Seeley WW, Menon V, Schatzberg AF, Keller J, Glover GH, Kenna H, Reiss AL, GreiciusMD (2007) Dissociable intrinsic connectivity networks for salience processing and executive control. J Neurosci 27:2349 -2356. CrossRef Medline
48. Serra L, Montagna P, Mignot E, Lugaresi E, Plazzi G (2008) Cataplexy features in childhood narcolepsy. Mov Disord 23:858-865. CrossRef Medline
49. Szameitat DP, Kreifelts B, Alter K, Szameitat AJ, Sterr A, Grodd W, Wildgruber D (2010) It is not always tickling: distinct cerebral responses during perception of different laughter types. Neuroimage 53:1264 -1271. CrossRef Medline
50. Thannickal TC, Moore RY, Nienhuis R, Ramanathan L, Gulyani S, Aldrich M, Cornford M, Siegel JM (2000) Reduced number of hypocretin neurons in human narcolepsy. Neuron 27:469-474. CrossRef Medline
51. Tucci V, Stegagno L, Vandi S, Ferrillo F, Palomba D, Vignatelli L, Ferini- Strambi L, Montagna P, Plazzi G (2003) Emotional information processing in patients with narcolepsy: a psychophysiologic investigation. Sleep 26:558 -564. Medline
52. Vassalli A, Dellepiane JM, Emmenegger Y, Jimenez S, Vandi S, Plazzi G, Franken P, TaftiM (2012) Electroencephalogram paroxysmal _ characterizes cataplexy in mice and children. Brain 136:1592-1608. CrossRef Medline
53. Vaudano AE, Ruggieri A, Tondelli M, Avanzini P, Benuzzi F, Gessaroli G,Cantalupo G, Mastrangelo M, Vignoli A, Bonaventura CD, Canevini MP, Bernardina BD, Nichelli PF, Meletti S (2014) The visual system in eyelid myoclonia with absences. Ann Neurol 76:412- 427. CrossRef Medline
54. Vetrugno R, D'Angelo R, Moghadam KK, Vandi S, Franceschini C, Mignot E, Montagna P, Plazzi G (2010) Behavioural and neurophysiological correlates of human cataplexy: a video-polygraphic study. Clin Neurophysiol 121:153-162. CrossRef Medline
55. Watson KK, Matthews BJ, Allman JM (2007) Brain activation during sight gags and language-dependent humor. Cereb Cortex 17:314 -324. CrossRef Medline
56. Wattendorf E, Westermann B, Fiedler K, Kaza E, Lotze M, Celio MR (2013) Exploration of the neural correlates of ticklish laughter by functional magnetic resonance imaging. Cereb Cortex 23:1280 -1289. CrossRef Medline