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Abstract

Background: The interrelationships among humor, smiling, and grinning have fascinated philosophers for millennia and neurologists for over a century. A functional dissociation between emotional facial expressions and those under voluntary control was suggested decades ago. Recent functional imaging studies, however, have been somewhat at odds with older studies with respect to the role of the right frontal cortex in the perception of humor.
Methods: Blood oxygen level–dependent (BOLD) activity was measured in 13 subjects during the presentation of “funny” vs “nonfunny” versions of essentially the same cartoons and compared with BOLD activity associated with “merely grinning” at similar nonfunny cartoons via fMRI.
Results: Humor perception was correlated with BOLD activity in the left temporo-occipitoparietal junction and left prefrontal cortex and humor-associated smiling (recorded with an MR-compatible video camera) with bilateral activity in the basal temporal lobes. Unexpectedly, both conditions were also accompanied by a decrease in BOLD activity in the right orbitofrontal cortex. Voluntary “grinning” in the absence of humorous stimuli was accompanied by bilateral activity in the facial motor regions.
Conclusions: These results confirm the clinically derived hypothesis of separate cortical regions responsible for the production of emotionally driven vs voluntary facial expressions. The right orbitofrontal decrease reconciles inconsistencies between clinical and functional imaging findings and may reflect a disinhibition of facial emotional expression.

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References

1.
Martin R. Approaches to the sense of humor: a historical review. In: Ruch W, ed. The sense of humor. New York: Mouton de Gryter, 1998:16–60.
2.
Wild B, Rodden FA, Grodd W, Ruch W. Neural correlates of laughter and humour: a review. Brain 2003;126:2121–2138.
3.
Gardner H, Ling PK, Flamm L, Silverman J. Comprehension and appreciation of humorous material following brain damage. Brain 1975;98:399–412.
4.
Shammi P, Stuss DT. Humour appreciation: a role of the right frontal lobe. Brain 1999;122:657–666.
5.
Wild B, Erb M, Lemke N, Scholz P, Bartels M, Grodd W. Video camera and light system for application in magnetic resonance scanners. Magn Res Imag 2000;18:893–896.
6.
Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 1994;18:192–205.
7.
Ruch W. Die Emotion Erheiterung: Ausdrucksformen und Bedingungen. Department of Psychology, University of Düsseldorf, 1990.
8.
Magnus A. Fall von Aufhebung des Willenseinflusses auf einige Hirnnerven. In: Müller J, ed. Archiv für Anatomie, Physiologie und Wissenschaftliche Medicin. Berlin: Verlag von W. Thome, 1837:258–266.
9.
Hopf HC, Muller FW, Hopf NJ. Localization of emotional and volitional facial paresis. Neurology 1992;42:1918–1923.
10.
Poeck K. Pathophysiology of emotional disorders associated with brain damage. In: Vinken, PJ, Bruyn GW, eds. Handbook of clinical neurology. Amsterdam: Elsevier, 1985:343–367.
11.
Weller M. Anterior opercular cortex lesions cause dissociated lower cranial nerve palsies and anarthria but no aphasia: Foix–Chavany–Marie syndrome and “automatic voluntary dissociation” revisited. J Neurol 1993;240:199–208.
12.
Goel V, Dolan RJ. The functional anatomy of humor: segregating cognitive and affective components. Nat Neurosci 2001;4:237–238.
13.
Iwase M, Ouchi Y, Okada H, et al. Neural substrates of human facial expression of pleasant emotion induced by comic films: a PET study. Neuroimage 2002;17:758–768.
14.
Mobbs D, Greicius MD, Abdel-Azim E, Menon V, Reiss AL. Humor modulates the mesolimbic reward centers. Neuron 2003;40:1041–1048.
15.
Moran JM, Wig GS, Adams RB, Janata P, Kelley WM. Neural correlates of humor detection and appreciation. Neuroimage 2004;21:1055–1060.
16.
Karama S, Roch Lecours A, Leroux J-M, et al. Areas of brain activation in males and females during viewing of erotic film excerpts. Hum Brain Map 2002;16:1–13.
17.
Brunet E, Sarfati Y, Hardy-Baylé M-C, Decety J. A PET investigation of the attribution of intentions with a nonverbal task. Neuroimage 2000;11:157–166.
18.
Blakemore SJ, Fonlupt P, Pachot Clouard M, et al. How the brain perceives causality: an event-related fMRI study. Neuroreport 2001;12:3741–3746.
19.
Peretz I, Zatorre RJ. The cognitive science of music. Oxford: Oxford University Press, 2003.
20.
Ozawa F, Matsuo K, Kato C, et al. The effects of listening comprehension of various genres of literature on response in the linguistic area: an fMRI study. Neuroreport 2000;11:1141–1143.
21.
Bookheimer S. Functional MRI of language: new approaches to understanding the cortical organization of semantic processing. Annu Rev Neurosci 2002;25:151–188.
22.
Martin A, Chao L. Semantic memory and the brain: structure and processes. Curr Opin Neurobiol 2001;11:194–211.
23.
Rapp A, Leube D, Erb M, Bartels M, Grodd W, Kircher T. Neural correlates of metaphor processing. Cogn Brain Res 2004;20:395–402.
24.
Phan KL, Wager T, Taylor SF, Liberzon I. Functional neuroanatomy of emotion: a meta-analysis of emotion activation studies in PET and fMRI. Neuroimage 2002;16:331–348.
25.
Wild B, Erb M, Eyb M, Bartels M, Grodd W. Why are smiles contagious? An fMRI study of the interaction between perception of facial affect and facial movements. Psychiatry Res Neuroimag 2003;123:17–36.
26.
Molinuevo JL, Arroyo S. Ictal smile. Epilepsia 1998;39:1357–1360.
27.
Coria F, Bahillo ME, Moral BM, Garcia GP, Ortiz SdSMR. Late-onset isolated gelastic epilepsy secondary to entrapment of the right temporal horn. Neurologia 2000;15:204–207.
28.
Arroyo S, Lesser RP, Gordon B, et al. Mirth, laughter and gelastic seizures. Brain 1993;116:757–780.
29.
Goldin PR, Hutcherson CAC, Ochsner KN, et al. The neural basement of amusement and sadness: a comparison of block contrast and subject-specific emotion intensity regression approaches. Neuroimage 2005;27:25–36.
30.
Wapner W, Hamby S, Gardner H. The role of the right hemisphere in the apprehension of complex linguistic material. Brain Lang 1981;14:15–33.
31.
Harel N, Lee S-P, Nagaoka T, Kim D-S, Kim S-G. Origin of negative blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 2002;22:908–917.
32.
Zaidel E, Kasher A, Soroker N, Batori E. Effects of right and left hemisphere damage on performance of the “Right Hemisphere Communication Battery.” Brain Lang 2002;80:510–535.
33.
Ironside R. Disorders of laughter due to brain lesions. Brain 1956;79:589–609.
34.
Zeilig G, Drubach DA, Katz ZM, Karatinos J. Pathological laughter and crying in patients with closed traumatic brain injury. Brain Injury 1996;10:591–597.
35.
Mendez MF, Nakawatase TV, Brown CV. Involuntary laughter and inappropriate hilarity. J Neuropsychiatry Clin Neurosci 1999;11:253–258.
36.
George MS, Ketter TA, Parekh PI, Horwitz B, Herscovitch P, Post RM. Brain activity during transient sadness and happiness in healthy women. Am J Psychiatry 1995;152:341–351.
37.
Franks NP, Lieb WR. A serious target for laughing gas. Nat Med 1998;4:383–384.

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Published In

Neurology®
Volume 66Number 6March 28, 2006
Pages: 887-893
PubMed: 16567707

Publication History

Published online: March 27, 2006
Published in print: March 28, 2006

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Authors

Affiliations & Disclosures

B. Wild, Privatdozentin Dr Med
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.
F. A. Rodden, PhD
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.
A. Rapp, Dr Med
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.
M. Erb, Dr Rer Nat
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.
W. Grodd, Prof Dr Med
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.
W. Ruch, Prof Dr Phil
From the Department of Psychiatry (B.W., A.R.) and Section for Experimental Magnetic Resonance of the CNS (B.W., F.A.R., A.R., M.E.,W.G.), Department of Neuroradiology, University of Tübingen, Germany; and Department of Psychology (W.R.), University of Zurich, Switzerland.

Notes

Address correspondence and reprint requests to Dr. B. Wild, Zwingerweg 1, 72202 Nagold, Germany; e-mail: [email protected]

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