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A Systematic Review of the Neural Correlates of Positive Emotions Leonardo Machado, Amaury Cantilino

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A Systematic Review of the Neural Correlates of Positive Emotions Leonardo Machado, Amaury Cantilino Revista Brasileira de Psiquiatria. 2017;39:172–179 Associac¸a˜ o Brasileira de Psiquiatria doi:10.1590/1516-4446-2016-1988 REVIEW ARTICLE A systematic review of the neural correlates of positive emotions Leonardo Machado, Amaury Cantilino Programa de Po´s-Graduac¸a˜o em Neuropsiquiatria e Cieˆncias do Comportamento, Universidade Federal de Pernambuco (UFPE), Recife, PE, Brazil. Objective: To conduct a systematic literature review of human studies reporting neural correlates of positive emotions. Methods: The PubMed and Web of Science databases were searched in January 2016 for scientific papers written in English. No restrictions were placed on year of publication. Results: Twenty-two articles were identified and 12 met the established criteria. Five had been published during the last 4 years. Formation and regulation of positive emotions, including happiness, are associated with significant reductions in activity in the right prefrontal cortex and bilaterally in the temporoparietal cortex, as well as with increased activity in the left prefrontal regions. They are also associated with increased activity in the cingulate gyrus, inferior and middle temporal gyri, amygdalae, and ventral striatum. Conclusion: It is too early to claim that there is an established understanding of the neuroscience of positive emotions and happiness. However, despite overlap in the brain regions involved in the formation and regulation of positive and negative emotions, we can conclude that positive emotions such as happiness activate specific brain regions. Keywords: Emotions; happiness; electroencephalography; neuroimaging Introduction theories about emotions have been proposed. Never- theless, it can be said that emotion describes a neural According to the philosopher Seneca, the most difficult impulse that moves an organism to action, whereas question is not who wants to be happy, but what makes a emotional feelings describes the subset of feelings that happy life.1 This was one of the great preoccupations of are associated with brain-body interactions, their neural post-Socratic philosophers and perhaps remains one of representations, and their expression.16 Interest in and the main issues in philosophy even now. A new concept data on the neural correlates of emotion and emotional of social development was introduced in 1972 as a result feelings have increased dramatically16,18 since Broca’s of work promoted by the king of Bhutan: gross national pioneering work on the great limbic lobe (1878) and happiness (GNH), intended as a counterbalance to the Papez’s proposal that there was a brain circuit respon- emphasis on measuring a country’s success in terms sible for emotions (1937). 2,3 of gross domestic product (GDP). Years later, when Basic emotions (expression, objective phenomena) and Seligman was president of the American Psychological emotional feelings (experience, subjective phenomena) Association, a new branch of psychology was established. are similar between individuals and across cultures.16 Positive psychology is the study of the virtues and strengths Thus, Ekman posited that there are six basic emotions: 4,5 of humans. Recently, more psychiatric research has been happiness, sadness, anger, disgust, fear, and surprise, in conducted into the relationship between personality traits addition to a neutral state.17 More recent studies indicate 6 and well-being, happiness and satisfaction with life in otherwise. The 10 most commonly reported categories of 7,8 psychiatrists, the implications of studies on happiness for emotions and emotional feelings can be organized into six 9-12 psychiatry, and subjective well-being in patients on anti- families: happiness (comprising happiness, joy, and con- 13 psychotics. In 2015, a new, correlate field has emerged tentment), anger (comprising anger, irritation, and frustra- within psychiatry: positive psychiatry, which shares with tion), anxiety, sadness, stress, and despair.16 positive psychology (among other factors) the study of 14,15 One of the theories that attempts to categorize emotion positive emotions, such as happiness. and emotional feelings is based on valence (positive and Although emotions are a universal phenomenon, there 16 16,17 negative). One of the most studied positive emotions is no consensus about their classification. Over 150 has been happiness, a subjective experience of great importance to humans. Recent research indicates that happiness is related to many psychosocial factors11; how- Correspondence: Leonardo Machado, Rua Frei Matias Teves, 280/ ever, individual-level factors, such as genetics19-21 and 114, CEP 50070-450, Recife, PE, Brazil, 6 E-mail: [email protected] personality traits, only predict about 35-50% of variance Submitted Apr 21 2016, accepted Jun 14 2016, Epub Nov 24 2016. in happiness.22,23 Investigating the neural correlates of Neural correlates of positive emotions 173 positive emotions, including happiness, seems to offer a techniques to investigate neural correlates of positive way of answering fundamental questions, such as why emotions, including happiness. The exclusion criteria some people feel happy and others do not. Although were: review articles, theoretical articles, animal studies, research on the neurobiology of pleasure,24 affective studies about neural correlates of subjective well-being, style,25 and resilience26 is relevant here, in recent years it and studies not directly related to neural correlates of has become possible to investigate brain structures rela- positive emotions or happiness (Figure 1). Using these ted to the construct of positive emotions27 using imaging criteria, 10 of the 22 retrieved articles were excluded; the techniques. remaining 12 form the basis of this review (Table 1). The purpose of this article is to review the progress made in the neuroscience of positive emotions as a result of research based on using neuroimaging or electro- encephalographic (EEG) techniques to investigate neural Results correlates of positive emotions, including happiness. In contrast to abundant data on the structural and functional brain changes associated with psychiatric Methods disorders and negative emotions, there is relatively little data on brain changes associated with normal emotional The search for papers was conducted in January 2016 in states and positive emotions; however, in recent years, two different databases, MEDLINE and Web of Science. there has been growing interest in the neural correlates of The following keywords were used in both databases: happiness. Of the 12 articles included in this review, five ‘‘neural correlates and positive emotions,’’ ‘‘neurobiology were published during the last 4 years. and positive emotions,’’ ‘‘neurobiology and happiness,’’ The oldest study included in this review was published ‘‘neural correlates and happiness,’’ and ‘‘neuroscience in 1995 in the American Journal of Psychiatry. Eleven and happiness.’’ Each of these combinations comprised healthy adult women with no history of mental illness were 15 an individual search query. Keywords had to appear in the scanned by using H2 O positron emission tomography title or abstract and the search was restricted to publica- (PET) during happy, sad, and neutral states induced by tions written in English. No restrictions were placed on recalling affect-appropriate life events and looking at year of publication. happy, sad, or neutral human faces. Emotional changes The inclusion criterion for this systematic review was: across tasks were assessed using paired, two-tailed original articles dealing with use of neuroimaging or EEG Student’s t tests to compare scores on the Positive Figure 1 Flow diagram of search strategy. Rev Bras Psiquiatr. 2017;39(2) 174 L Machado & A Cantilino Table 1 Description of results Author Year Sample Main findings Main limitations George28 1995 11 healthy and never 1) Transient sadness activated bilateral limbic 1) Small sample mentally ill adult women and paralimbic structures (right medial frontal 2) Only women participated gyrus, left dorsolateral prefrontal cortex, bilateral 3) Many memories are cingulate gyrus, caudate, putamen, thalamus, emotionally mixed. Sadness and fornix, left insula, and left midline cerebellum). happiness are not necessarily 2) Transient happiness was associated with mutually exclusive significant and widespread reductions in cortical regional cerebral blood flow, especially in the right prefrontal and bilateral temporoparietal regions. Lane29 1997 12 healthy women 1) Happiness, sadness, and disgust were each 1) Small sample associated with increases in activity in the 2) Only women participated thalamus and medial prefrontal cortex (BA9). 2) Happiness, sadness, and disgust were also associated with activation of anterior and posterior temporal structures. 3) Recalled sadness was associated with increased activation in the anterior insula. 4) Happiness was distinguished from sadness by greater activity in the vicinity of the ventral medial frontal cortex. Pelletier30 2003 Nine professional actors Relative to an emotionally neutral state, both sad 1) Small sample and happy states were associated with significant 2) Sample limited to professionally loci of activation, bilaterally, in the orbitofrontal trained (i.e., expert) individuals, cortex and in the left medial prefrontal cortex, left which may present certain ventrolateral prefrontal cortex, left anterior problems, given that distinctions temporal pole, and right pons. between experts and typical untrained individuals can be quite marked
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