Neural pathways underlying the interplay between emotional experience and behavior, from old theories to modern insight

Authors

  • Olivera Stanojlović Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Belgrade University, Višegradska 26, 11000 Belgrade, Serbia https://orcid.org/0000-0001-5317-3827
  • Nikola Šutulović Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Belgrade University, Višegradska 26, 11000 Belgrade, Serbia https://orcid.org/0000-0002-9499-3247
  • Dragan Hrnčić Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Belgrade University, Višegradska 26, 11000 Belgrade, Serbia https://orcid.org/0000-0003-0806-444X
  • Dušan Mladenović Institute of Pathophysiology “Ljubodrag Buba Mihailović”, Faculty of Medicine, Belgrade University, 9 Dr Subotića 9, 11000 Belgrade, Serbia https://orcid.org/0000-0002-8921-6232
  • Aleksandra Rašić-Marković Institute of Medical Physiology “Richard Burian”, Faculty of Medicine, Belgrade University, Višegradska 26, 11000 Belgrade, Serbia https://orcid.org/0000-0003-1131-2328
  • Nebojša Radunović Serbian Academy of Sciences and Arts, Kneza Mihaila 35, 11 000 Belgrade, Serbia
  • Milena Vesković Institute of Pathophysiology “Ljubodrag Buba Mihailović”, Faculty of Medicine, Belgrade University, 9 Dr Subotića 9, 11000 Belgrade, Serbia https://orcid.org/0000-0002-7505-5466

DOI:

https://doi.org/10.2298/ABS210510029S

Keywords:

emotions, amygdala, prefrontal cortex, top-down, bottom-up

Abstract

Paper description:

  • The historical development of the perception of emotions from the beginning of emotion elucidation to contemporary theories of doctors, neuropsychologists, neuroscientists, neurologists and psychiatrists are examined.
  • Modern theories are surveyed by a bottom-up approach, a stimulus-focused view of emotional processing that considers the stimulation of the amygdala which recognizes affectively visible stimuli, creating behavioral and visceral responses, and a top-down approach, a cognition-focused view of emotional processing that considers activation of the system for selective attention, working memory, speech, enabling conscious decisions to be made in different situations.

Abstract: Emotions are specific psychological states brought about by neurophysiological changes associated with feelings, thoughts and behavioral responses. Emotions were considered as irrational experiences beyond the domain of logical perception because of their intertwinement with mood, temperament, creativity, motivation and personality. Through the centuries, emotions have been the focus of research among great classical philosophers, doctors, neuropsychologists, neuroscientists, neurologists and psychiatrists. The neurophysiological basis of behavior, such as emotional facial expression, and autonomic events in the physiological theory of William James and James-Lange and modified by Cannon-Bard, was followed by the two-factor theory of emotions of Schachter-Singer and Lazarus’ higher-order cognitive evaluation. Four components that influence each other represent the concept of emotions and complete the overall emotional experience, and these are: autonomous (increase in heart rate, blood pressure); somatic (body language, facial expressions); cognitive (control, management), and subjective feeling (emotion, individual experience). The interplay between emotions and cognition has been the subject of research. Emotions can be evoked reflexively by simple physical stimuli (bottom-up), but can also be complex reactions involving cognitive, physiological and behavioral reactions (top-down). The amygdala, the “alert" or “neural alarm” structure, is responsible for conditioning fear, while the medial prefrontal cortex participates in emotion self-regulation and decision making.

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References

De Sousa R. I-Ronald de Sousa. Arist Soc Suppl Vol. 2002;76(1):247-63. https://doi.org/10.1111/1467-8349.00098

Mulligan K, Scherer KR. Toward a Working Definition of Emotion. Emotion Review. 2012;4(4):345-57. https://doi.org/10.1177/1754073912445818

Dillon J. Shadows on the Soul: Plotinian Approaches to a Solution of the Mind-Body Problem. In: Karfík F, Song E, editors. Plato Revived. Berlin: De Gruyter; 2013. p.73-84. https://doi.org/10.1515/9783110324662.73

Rankov Petrovic B, Hrncic D, Mladenovic D, Simic T, Suvakov S, Jovanovic D, Puskas N, Zaletel I, Velimirovic M, Cirkovic V, Macut D, Stanojlovic O, Rasic-Markovic A. Prenatal Androgenization Induces Anxiety-Like Behavior in Female Rats, Associated with Reduction of Inhibitory Interneurons and Increased BDNF in Hippocampus and Cortex. Biomed Res Int. 2019;2019:3426092. https://doi.org/10.1155/2019/3426092

Bonanno GA, Keltner D. Facial expressions of emotion and the course of conjugal bereavement. J Abnorm Psychol. 1997;106(1):126-37. https://doi.org/10.1037/0021-843X.106.1.126

Siddiqui SV, Chatterjee U, Kumar D, Siddiqui A, Goyal N. Neuropsychology of prefrontal cortex. Indian J Psychiatry. 2008;50(3):202-8. https://doi.org/10.4103/0019-5545.43634

Ekman P, Friesen WV. Constants across cultures in the face and emotion. J Pers Soc Psychol. 1971;17(2):124-9. https://doi.org/10.1037/h0030377

Pace-Schott EF, Amole MC, Aue T, Balconi M, Bylsma LM, Critchley H, Demaree HA, Friedman BH, Gooding AEK, Gosseries O, Jovanovic T, Kirby LAJ, Kozlowska K, Laureys S, Lowe L, Magee K, Marin MF, Merner AR, Robinson JL, Smith RC, Spangler DP, Van Overveld M, VanElzakker MB. Physiological feelings. Neurosci Biobehav Rev. 2019;103:267-304. https://doi.org/10.1016/j.neubiorev.2019.05.002

Schachter S, Singer JE. Cognitive, social, and physiological determinants of emotional state. Psychol Rev. 1962;69:379-99. https://doi.org/10.1037/h0046234

Davis JI, Senghas A, Ochsner KN. How Does Facial Feedback Modulate Emotional Experience? J Res Pers. 2009;43(5):822-29. https://doi.org/10.1016/j.jrp.2009.06.005

Hrncic D, Mikić J, Rasic-Markovic A, Velimirović M, Stojković T, Obrenović R, Rankov-Petrović B, Šušić V, Djuric D, Petronijević N, Stanojlovic O. Anxiety-related behavior in hyperhomocysteinemia induced by methionine nutritional overload in rats: role of the brain oxidative stress. Can J Physiol Pharmacol. 2016;94(10):1074-82. https://doi.org/10.1139/cjpp-2015-0581

LeDoux J. The emotional brain, fear, and the amygdala. Cell Mol Neurobiol. 2003;23(4-5):727-38. https://doi.org/10.1023/a:1025048802629

Hunt C, Keogh E, French CC. Anxiety sensitivity: the role of conscious awareness and selective attentional bias to physical threat. Emotion. 2006;6(3):418-28. https://doi.org/10.1037/1528-3542.6.3.418

Yiend J. The effects of emotion on attention: A review of attentional processing of emotional information. Cogn Emot. 2010;24(1):3-47. https://doi.org/10.1080/02699930903205698

Waterman AS. The relevance of Aristotle's conception of eudaimonia for the psychological study of happiness. J Theor Philos Psychol. 1990;10,39-44. https://doi.org/10.1037/h0091489

Boeri MD, Kanayama YY, Mittelmann J. Soul and Mind in Greek Thought. Psychological Issues in Plato and Aristotle. Springer International Publishing; 2018. 251 p. https://doi.org/10.1007/978-3-319-78547-9

Kandel ER, Squire LR. Neuroscience: breaking down scientific barriers to the study of brain and mind. Science. 2000;290(5494):1113-20. https://doi.org/10.1126/science.290.5494.1113

Roxo MR, Franceschini PR, Zubaran C, Kleber FD, Sander JW. The limbic system conception and its historical evolution. ScientificWorldJournal. 2011;11:2428-41. https://doi.org/10.1100/2011/157150

Bennett MR. The early history of the synapse: from Plato to Sherrington. Brain Res Bull. 1999;50(2):95-118. https://doi.org/10.1016/S0361-9230(99)00094-5

Barrett LF. Psychological Construction: The Darwinian Approach to the Science of Emotion. Emotion Review. 2013;5(4):379-89. https://doi.org/10.1177/1754073913489753

Darwin C. A biographical sketch of an infant. Mind. 1877;2:285-94. https://doi.org/10.1093/mind/os-2.7.285

Darwin C. The descent of man, and selection in relation to sex. London: J. Murray; 1871. https://doi.org/10.5962/bhl.title.2092

Esperidião-Antonio V, Majeski-Colombo M, Toledo-Monteverde D, Moraes-Martins G, Fernandes JJ, Bauchiglioni de Assis M, Montenegro S, Siqueira-Batista R. Neurobiology of emotions: an update. Int Rev Psychiatry. 2017;29(3):293-307. https://doi.org/10.1080/09540261.2017.1285983

Skinner BF. Superstition in the pigeon. J Exp Psychol. 1948;38(2):168-72. https://doi.org/10.1037/h0055873

Ochsner KN, Gross JJ. The cognitive control of emotion. Trends Cogn Sci. 2005;9(5):242-9. https://doi.org/10.1016/j.tics.2005.03.010

Barrett LF, Satpute AB. Historical pitfalls and new directions in the neuroscience of emotion. Neurosci Lett. 2019;693:9-18. https://doi.org/10.1016/j.neulet.2017.07.045

Fridlund AJ, Beck HP, Goldie WD, Irons G. Little Albert: A neurologically impaired child. Hist Psychol. 2012;15(4):302-27. https://doi.org/10.1037/a0026720

Harris B. Letting go of little Albert: disciplinary memory, history, and the uses of myth. J Hist Behav Sci. 2011;47(1):1-17. https://doi.org/10.1002/jhbs.20470

Lashley KS, Wade M. The Pavlovian theory of generalization. Psychol Rev. 1946;53:72-87. https://doi.org/10.1037/h0059999

Marasanov AV, Valtseva EA. [Scientific potential of phenomics - functional direction of genetics]. Gig Sanit. 2016;95(9):805-10. Russian. https://doi.org/10.18821/0016-9900-2016-95-9-805-810

Selye H. A syndrome produced by diverse nocuous agents. 1936. J Neuropsychiatry Clin Neurosci. 1998;10(2):230-1. https://doi.org/10.1176/jnp.10.2.230a

Leblanc R. Pavlov, Penfield, and the physiology of the mind. Neurology. 2019;92(12):575-578. https://doi.org/10.1212/WNL.0000000000007145

Stanojlović OP, Hrncić DR, Zivanović DP, Susić VT. Anticonvulsant, but not antiepileptic, action of valproate on audiogenic seizures in metaphit-treated rats. Clin Exp Pharmacol Physiol. 2007;34(10):1010-5. https://doi.org/10.1111/j.1440-1681.2007.04681.x

Ekman P. What We Become Emotional About. In: Manstead ASR, Frijda N, Fischer A, editors. Feelings and Emotions. Cambridge: Cambridge University Press; 2004. p. 119-35. https://doi.org/10.1017/CBO9780511806582.008

Rosenberg EL, Ekman P, Jiang W, Babyak M, Coleman RE, Hanson M, O'Connor C, Waugh R, Blumenthal JA. Linkages between facial expressions of anger and transient myocardial ischemia in men with coronary artery disease. Emotion. 2001;1(2):107-15. https://doi.org/10.1037/1528-3542.1.2.107

James W. Pragmatism: A new name for some old ways of thinking. New York: Longmans, Green and Co,; 1907. https://doi.org/10.1037/10851-000

James, W. What is an Emotion? Mind. 1884;9(34):188-205. https://doi.org/10.1093/mind/os-IX.34.188

Cannon WB. The James-Lange theory of emotions: a critical examination and an alternative theory. Am J Psychol. 1987;100(3-4):567-86. https://doi.org/10.2307/1422695

Friedman BH. Feelings and the body: the Jamesian perspective on autonomic specificity of emotion. Biol Psychol. 2010;84(3):383-93. https://doi.org/10.1016/j.biopsycho.2009.10.006

Cannon WB. Again the James-Lange and the thalamic theories of emotion. Psychol Rev. 1931;38(4):281-95. https://doi.org/10.1037/h0072957

Coleman AE, Snarey J. James-Lange Theory of Emotion. In: Goldstein S, Naglieri JA, editors. Encyclopedia of Child Behavior and Development. Boston, MA: Springer US,; 2011. p. 844-6. https://doi.org/10.1007/978-0-387-79061-9_3146

Bard P. A diencephalic mechanism for the expression of rage with special reference to the sympathetic nervous system. Am J Physiol-Leg Content. 1928;84(3):490-515. https://doi.org/10.1152/ajplegacy.1928.84.3.490

Cannon WB. "Voodoo" death. Am Anthropol. 1942;44:169-181. https://doi.org/10.1525/aa.1942.44.2.02a00010

Child ND, Benarroch EE. Anterior nucleus of the thalamus: functional organization and clinical implications. Neurology. 2013;81(21):1869-76. https://doi.org/10.1212/01.wnl.0000436078.95856.56

MacLEAN PD. Psychosomatic disease and the visceral brain; recent developments bearing on the Papez theory of emotion. Psychosom Med. 1949;11(6):338-53. https://doi.org/10.1097/00006842-194911000-00003

Maia TV. Two-factor theory, the actor-critic model, and conditioned avoidance. Learn Behav. 2010;38(1):50-67. https://doi.org/10.3758/LB.38.1.50

Ekman P, Campos J. Richard Stanley Lazarus (1922-2002). Am Psychol. 2003;58(9):756-7. https://doi.org/10.1037/0003-066X.58.9.756

Folkman S, Lazarus RS. An analysis of coping in a middle-aged community sample. J Health Soc Behav. 1980;21(3):219-39. https://doi.org/10.2307/2136617

Lazarus RS. A cognitively oriented psychologist looks at biofeedback. Am Psychol. 1975;30(5):553-61. https://doi.org/10.1037/h0076649

Stanojlović O, Rasić-Marković A, Hrncić D, Susić V, Macut D, Radosavljević T, Djuric D. Two types of seizures in homocysteine thiolactone-treated adult rats, behavioral and electroencephalographic study. Cell Mol Neurobiol. 2009;29(3):329-39. https://doi.org/10.1007/s10571-008-9324-8

Stanojlović O, Nikolić T, Hrnčić D, Radonjić N, Rašić-Marković A, Mladenović D, Petronijević N. Ontogenetic influence on rat susceptibility to lindane seizure after pretreatment with phencyclidine. Environ Toxicol Pharmacol. 2013;35(2):161-70. https://doi.org/10.1016/j.etap.2012.12.006

McRae K, Jacobs SE, Ray RD, John OP, Gross JJ. Individual differences in reappraisal ability: Links to reappraisal frequency, well-being, and cognitive control. J Res Pers. 2012;46(1): 2-7. https://doi.org/10.1016/j.jrp.2011.10.003

McRae K, Misra S, Prasad AK, Pereira SC, Gross JJ. Bottom-up and top-down emotion generation: implications for emotion regulation. Soc Cogn Affect Neurosci. 2012;7(3):253-62. https://doi.org/10.1093/scan/nsq103

Simpson JR, Ongür D, Akbudak E, Conturo TE, Ollinger JM, Snyder AZ, Gusnard DA, Raichle ME. The emotional modulation of cognitive processing: an fMRI study. J Cogn Neurosci. 2000;12 Suppl 2:157-70. https://doi.org/10.1162/089892900564019

Gross JJ. The Emerging Field of Emotion Regulation: An Integrative Review. Rev Gen Psychol. 1998;2(3):271-99. https://doi.org/10.1037/1089-2680.2.3.271

Otto B, Misra S, Prasad A, McRae K. Functional overlap of top-down emotion regulation and generation: an fMRI study identifying common neural substrates between cognitive reappraisal and cognitively generated emotions. Cogn Affect Behav Neurosci. 2014;14(3):923-38. https://doi.org/10.3758/s13415-013-0240-0

Zilverstand A, Parvaz MA, Goldstein RZ. Neuroimaging cognitive reappraisal in clinical populations to define neural targets for enhancing emotion regulation. A systematic review. Neuroimage. 2017;151:105-16. https://doi.org/10.1016/j.neuroimage.2016.06.009

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Published

2021-10-12

How to Cite

1.
Stanojlović O, Šutulović N, Hrnčić D, Mladenović D, Rašić-Marković A, Radunović N, Vesković M. Neural pathways underlying the interplay between emotional experience and behavior, from old theories to modern insight. Arch Biol Sci [Internet]. 2021Oct.12 [cited 2024Nov.21];73(3):361-70. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/6583

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Vol. 73 No. 3 (2021)

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