Right hemisphere has the last laugh: neural dynamics of joke appreciation.
Understanding a joke relies on semantic, mnemonic, inferential, and emotional contributions from multiple brain areas. Anatomically constrained magnetoencephalography (aMEG) combining high-density whole-head MEG with anatomical magnetic resonance imaging allowed us to estimate where the humor-specific brain activations occur and to understand their temporal sequence. Punch lines provided either funny, not funny (semantically congruent), or nonsensical (incongruent) replies to joke questions. Healthy subjects rated them as being funny or not funny. As expected, incongruous endings evoke the largest N400m in left-dominant temporo-prefrontal areas, due to integration difficulty. In contrast, funny punch lines evoke the smallest N400m during this initial lexical-semantic stage, consistent with their primed "surface congruity" with the setup question. In line with its sensitivity to ambiguity, the anteromedial prefrontal cortex may contribute to the subsequent "second take" processing, which, for jokes, presumably reflects detection of a clever "twist" contained in the funny punch lines. Joke-selective activity simultaneously emerges in the right prefrontal cortex, which may lead an extended bilateral temporo-frontal network in establishing the distant unexpected creative coherence between the punch line and the setup. This progression from an initially promising but misleading integration from left frontotemporal associations, to medial prefrontal ambiguity evaluation and right prefrontal reprocessing, may reflect the essential tension and resolution underlying humor.
Department of Radiology, University of California San Diego, 9500 Gilman Dr., 0841, La Jolla, CA 92093-0841, USA. xenia@ucsd.edu
Ksenija
K
Marinkovic
Sharelle
S
Baldwin
Maureen G
MG
Courtney
Thomas
T
Witzel
Anders M
AM
Dale
Eric
E
Halgren
D000328:Adult; D001931:Brain Mapping; D032882:Comprehension / Q000502:physiology*; D005071:Evoked Potentials / Q000502:physiology*; D007839:Functional Laterality / Q000502:physiology*; D006801:Humans; D007091:Image Processing, Computer-Assisted; D008279:Magnetic Resonance Imaging / Q000379:methods; D015225:Magnetoencephalography; D008297:Male; D017711:Nonlinear Dynamics; D012660:Semantics; D017603:Signal Detection, Psychological / Q000502:physiology; D013997:Time Factors; D014925:Wit and Humor as Topic; D055815:Young Adult
Brain Lang. 2007 Mar;100(3):223-37
16546247
Brain Lang. 2007 Feb;100(2):142-9
16677700
Brain Res. 2007 May 18;1146:23-49
17400197
Laterality. 2009 Jan;14(1):30-54
18608849
J Cogn Neurosci. 1993 Winter;5(1):34-44
23972118
Crit Rev Neurobiol. 2000;14(3-4):199-224
12645958
J Neurosci. 1995 Feb;15(2):1090-8
7869085
J Psycholinguist Res. 2002 Jan;31(1):45-63
11924839
Brain Lang. 1986 Mar;27(2):310-21
3955344
Brain. 1992 Dec;115 ( Pt 6):1783-806
1486461
Brain Lang. 2006 Jun;97(3):279-93
16343606
Brain Cogn. 1986 Oct;5(4):399-411
3580185
Psychol Rev. 1992 Oct;99(4):663-88
1454903
Nat Rev Neurosci. 2008 Dec;9(12):920-33
19020511
J Cogn Neurosci. 2005 Mar;17(3):494-506
15814008
J Physiol Paris. 1994;88(1):1-50
8019524
Psychon Bull Rev. 2004 Oct;11(5):882-8
15732698
Brain Res Cogn Brain Res. 1999 Oct 25;8(3):373-92
10556614
Brain Lang. 1998 Oct 1;64(3):377-408
9743549
Electroencephalogr Clin Neurophysiol. 1985 Apr;60(4):343-55
2579801
Neuron. 2003 May 8;38(3):487-97
12741994
Clin Neurosci. 1997;4(2):64-72
9059755
Brain Lang. 1993 Jan;44(1):80-120
8467379
Neuroimage. 2006 May 1;30(4):1401-13
16488158
Neuropsychologia. 2002;40(1):54-75
11595262
Brain Res Cogn Brain Res. 2005 Feb;22(2):241-55
15653297
Brain Lang. 1983 Jan;18(1):20-7
6839130
Hum Brain Mapp. 2002 Aug;16(4):251-61
12112766
JAMA. 1984 Dec 7;252(21):2995-8
6502861
Neuropsychologia. 1990;28(4):375-83
1692980
Neuroreport. 2000 Apr 27;11(6):1141-3
10817581
Brain Lang. 2003 Apr;85(1):1-36
12681346
Brain. 1999 Jan;122 ( Pt 1):61-73
10050895
Hum Brain Mapp. 2002 May;16(1):47-62
11870926
Hum Brain Mapp. 1999;8(4):272-84
10619420
Brain Cogn. 2005 Feb;57(1):70-83
15629218
Brain. 1999 Apr;122 ( Pt 4):657-66
10219779
J Cogn Neurosci. 2007 Jul;19(7):1193-205
17583994
Brain. 1975 Sep;98(3):399-412
1182484
Brain Lang. 2007 Mar;100(3):257-61
16919324
Philos Trans R Soc Lond B Biol Sci. 2007 May 29;362(1481):801-11
17412680
Neuroimage. 2002 Nov;17(3):1101-16
12414253
Neuroimage. 1999 Jul;10(1):1-5
10385576
Brain. 1998 Jun;121 ( Pt 6):1133-42
9648548
Nat Neurosci. 2001 Mar;4(3):237-8
11224538
J Neurosci. 1995 Feb;15(2):1080-9
7869084
IEEE Trans Biomed Eng. 1991 May;38(5):409-17
1874522
Psychophysiology. 1993 Jan;30(1):47-61
8416062
Brain Lang. 2007 Feb;100(2):115-26
16290261
Hum Brain Mapp. 1999;8(2-3):80-5
10524596
Neuropsychologia. 2000;38(11):1518-30
10906377
Brain. 2002 May;125(Pt 5):1125-36
11960901
Neuroimage. 1999 Feb;9(2):179-94
9931268
Science. 1980 Jan 11;207(4427):203-5
7350657
Trends Cogn Sci. 2003 Jul;7(7):293-299
12860187
Neuron. 2003 Dec 4;40(5):1041-8
14659102
J Cogn Neurosci. 2003 Jan 1;15(1):98-110
12590846
Brain Res. 2007 May 18;1146:115-27
17433891
Brain Res Cogn Brain Res. 2005 Dec;25(3):589-606
16202570
Brain Res. 2007 May 18;1146:75-84
16901469
J Cogn Neurosci. 1993 Spring;5(2):162-76
23972151
Neurology. 2006 Mar 28;66(6):887-93
16567707
Neuroscientist. 2005 Dec;11(6):563-76
16282597
Neuroimage. 2007 Sep 1;37(3):993-1004
17611124
Neuroimage. 2006 Oct 15;33(1):343-61
16876436
Brain Res Cogn Brain Res. 2003 Jun;17(1):117-29
12763198
J Cogn Neurosci. 2006 Nov;18(11):1789-98
17069470
Trends Cogn Sci. 2000 Jun;4(6):215-222
10827444
Neurosci Lett. 2001 Dec;316(2):71-4
11742718
Brain Lang. 2007 Mar;100(3):238-56
16412501
Brain Lang. 2009 Mar;108(3):184-90
18678402
Brain Lang. 1981 Sep;14(1):15-33
7272721
Brain Res Cogn Brain Res. 2005 Aug;24(3):691-701
15894468
Med Biol Eng Comput. 1994 Jan;32(1):35-42
8182960
Cogn Psychol. 2001 Jun;42(4):368-407
11368528
Brain Res. 2007 May 18;1146:128-45
17433892
Brain Lang. 2007 Feb;100(2):111-4
16956657
Neuron. 2001 Aug 2;31(2):329-38
11502262
Brain Res Cogn Brain Res. 2004 May;19(3):275-88
15062865
Annu Rev Neurosci. 2002;25:151-88
12052907
Neuroimage. 2006 Jan 15;29(2):536-44
16165371
Brain Res. 2006 Aug 23;1106(1):150-163
16843443
J Cogn Neurosci. 2006 Jul;18(7):1181-97
16839291
Med Hypotheses. 1998 Oct;51(4):351-4
9824844
Brain Lang. 1992 Apr;42(3):320-36
1606490
Brain Lang. 2002 Feb;80(2):188-207
11827443
Neuroscientist. 2004 Apr;10(2):142-52
15070488
Hum Brain Mapp. 2011 Aug;32(8):1260-76
20665718
Neuroimage. 2004 Mar;21(3):1055-60
15006673
Curr Neurol Neurosci Rep. 2004 Nov;4(6):466-70
15509448
Electroencephalogr Clin Neurophysiol. 1998 Jan;108(1):45-56
9474061
Brain Lang. 1998 Mar;62(1):89-106
9570881
Psychol Rev. 2001 Jul;108(3):624-52
11488380
Neuropsychologia. 2005;43(1):128-41
15488912
Electroencephalogr Clin Neurophysiol. 1986 Feb;63(2):145-59
2417815
Neuroimage. 2002 Nov;17(3):1599-612
12414298
Neuron. 2000 Apr;26(1):55-67
10798392
Brain Lang. 1990 Feb;38(2):315-33
2322815
Trends Cogn Sci. 2000 Dec 1;4(12):463-470
11115760
J Neurosci. 2001 May 15;21(10):3564-71
11331385
Q J Exp Psychol (Hove). 2007 Jun;60(6):779-89
17514594
J Exp Psychol Learn Mem Cogn. 1994 Jul;20(4):786-803
8064247
Neuroimage. 1999 Feb;9(2):195-207
9931269