Brain circuits signaling the absence of emotion in body language.

Publisher: National Academy of Sciences Country of Publication: United States NLM ID: 7505876 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1091-6490 (Electronic) Linking ISSN: 00278424 NLM ISO Abbreviation: Proc Natl Acad Sci U S A Subsets: MEDLINE

Original Publication: Washington, DC : National Academy of Sciences

Kinesics*; Emotions/*physiology ; Mental Disorders/*physiopathology; Adult ; Amygdala/physiology ; Brain/physiology ; Brain Mapping/methods ; Cerebral Cortex/physiology ; Facial Expression ; Humans ; Magnetic Resonance Imaging/methods ; Male ; Neural Pathways/physiology ; Photic Stimulation/methods

Adaptive social behavior and mental well-being depend on not only recognizing emotional expressions but also, inferring the absence of emotion. While the neurobiology underwriting the perception of emotions is well studied, the mechanisms for detecting a lack of emotional content in social signals remain largely unknown. Here, using cutting-edge analyses of effective brain connectivity, we uncover the brain networks differentiating neutral and emotional body language. The data indicate greater activation of the right amygdala and midline cerebellar vermis to nonemotional as opposed to emotional body language. Most important, the effective connectivity between the amygdala and insula predicts people's ability to recognize the absence of emotion. These conclusions extend substantially current concepts of emotion perception by suggesting engagement of limbic effective connectivity in recognizing the lack of emotion in body language reading. Furthermore, the outcome may advance the understanding of overly emotional interpretation of social signals in depression or schizophrenia by providing the missing link between body language reading and limbic pathways. The study thus opens an avenue for multidisciplinary research on social cognition and the underlying cerebrocerebellar networks, ranging from animal models to patients with neuropsychiatric conditions.
Competing Interests: The authors declare no competing interest.

Neuropsychologia. 2010 Oct;48(12):3416-29. (PMID: 20619280)
Science. 2020 Mar 20;367(6484):1282. (PMID: 32179702)
Cereb Cortex. 2015 Oct;25(10):3468-74. (PMID: 25100856)
Cognition. 2001 Dec;82(2):B51-61. (PMID: 11716834)
Cerebellum. 2007;6(3):254-67. (PMID: 17786822)
Proc Natl Acad Sci U S A. 2014 Jan 14;111(2):823-8. (PMID: 24297904)
Nat Rev Neurosci. 2010 Oct;11(10):697-709. (PMID: 20811475)
Proc Natl Acad Sci U S A. 2010 May 18;107(20):9400-5. (PMID: 20421469)
Neuroimage. 2012 Feb 1;59(3):2824-30. (PMID: 22019860)
Psychiatry Res. 2004 Sep 30;128(2):123-33. (PMID: 15488955)
Neuroimage. 2016 Mar;128:413-431. (PMID: 26569570)
Front Psychiatry. 2016 Jun 22;7:115. (PMID: 27445871)
Nat Methods. 2011 Jun 26;8(8):665-70. (PMID: 21706013)
Nat Rev Neurosci. 2010 Nov;11(11):773-83. (PMID: 20959860)
Front Psychol. 2019 Apr 24;10:904. (PMID: 31105624)
Proc Natl Acad Sci U S A. 2015 Dec 29;112(52):16012-7. (PMID: 26668400)
Hum Brain Mapp. 2013 Dec;34(12):3247-66. (PMID: 22806915)
Neuropsychologia. 2010 Mar;48(4):1144-59. (PMID: 20026086)
Nature. 1994 Dec 15;372(6507):669-72. (PMID: 7990957)
PLoS One. 2013 Nov 22;8(11):e81716. (PMID: 24278456)
Neuron. 2019 Aug 7;103(3):533-545.e5. (PMID: 31196672)
Front Psychol. 2011 Feb 02;2:16. (PMID: 21713180)
Brain Struct Funct. 2010 Jun;214(5-6):519-34. (PMID: 20512376)
Neuroimage. 2002 Jan;15(1):273-89. (PMID: 11771995)
Nat Neurosci. 2015 Sep;18(9):1310-7. (PMID: 26237366)
Nat Rev Neurosci. 2018 Jun;19(6):338-350. (PMID: 29643480)
J Neurosci. 2015 Sep 23;35(38):12994-3005. (PMID: 26400931)
Sci Rep. 2019 Jul 8;9(1):9849. (PMID: 31285532)
Brain. 1998 Apr;121 ( Pt 4):561-79. (PMID: 9577385)
Cereb Cortex. 2012 May;22(5):981-95. (PMID: 21775676)
Front Psychiatry. 2014 Feb 19;5:17. (PMID: 24600410)
J Neurosci. 2010 Jan 13;30(2):431-8. (PMID: 20071507)
J Comp Neurol. 1982 Nov 20;212(1):38-52. (PMID: 7174907)
Trends Cogn Sci. 2017 May;21(5):313-332. (PMID: 28385461)
J Neurosci Res. 2017 Jan 2;95(1-2):235-250. (PMID: 27688155)
Anim Cogn. 2010 May;13(3):555-64. (PMID: 20052512)
Int J Environ Res Public Health. 2020 Mar 19;17(6):. (PMID: 32204411)
Neuroimage. 2013 Dec;83:751-60. (PMID: 23876243)
Ann N Y Acad Sci. 2003 Apr;985:356-69. (PMID: 12724171)
Biol Psychiatry. 2013 Jan 1;73(1):85-92. (PMID: 22770651)
Cerebellum. 2009 Mar;8(1):28-34. (PMID: 18855096)
Neuron. 2009 Jun 25;62(6):757-71. (PMID: 19555645)
Brain Struct Funct. 2019 Jan;224(1):205-217. (PMID: 30302538)
Biol Psychol. 2019 Jul;145:211-223. (PMID: 31129312)
Curr Opin Neurobiol. 2008 Apr;18(2):166-72. (PMID: 18655833)
Proc Natl Acad Sci U S A. 2018 Dec 18;115(51):E12034-E12042. (PMID: 30514816)
Neuron. 1996 Nov;17(5):875-87. (PMID: 8938120)
Proc Natl Acad Sci U S A. 2010 Dec 7;107(49):21223-8. (PMID: 21078973)
Lancet. 2020 Mar 14;395(10227):912-920. (PMID: 32112714)
Nature. 1996 Oct 31;383(6603):812-5. (PMID: 8893004)
Annu Rev Neurosci. 2009;32:413-34. (PMID: 19555291)
Neuron. 2001 Jun;30(3):829-41. (PMID: 11430815)
Cereb Cortex. 2014 Mar;24(3):626-32. (PMID: 23169930)

United Kingdom WT_ Wellcome Trust; 088130/Z/09/Z United Kingdom WT_ Wellcome Trust

Keywords: body language; effective connectivity; emotion; social cognition

Date Created: 20200809 Date Completed: 20201028 Latest Revision: 20210206

20240628

PMC7456113

10.1073/pnas.2007141117

32764147