Review Love Is More Than Just a Kiss: a Neurobiological Perspective on Love and Affection
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Neuroscience 201 (2012) 114–124 REVIEW LOVE IS MORE THAN JUST A KISS: A NEUROBIOLOGICAL PERSPECTIVE ON LOVE AND AFFECTION A. DE BOER, E. M. VAN BUEL AND G. J. TER HORST* Gender differences in love 119 Neuroimaging Center, University Medical Center Groningen, Univer- The course of a relationship 120 sity Groningen, Antonius Deusinglaan 2, 9713 AW Groningen, The Phase 1: Being in love 120 Netherlands Phase 2: Passional love 120 Phase 3: Companionate love 120 Breakup of a relationship 121 Abstract—Love, attachment, and truth of human monogamy Human monogamy: truth or myth? 121 have become important research themes in neuroscience. Conclusion 122 After the introduction of functional Magnetic Resonance Im- Acknowledgments 122 aging (fMRI) and Positron Emission Tomography (PET), neu- References 122 roscientists have demonstrated increased interest in the neu- robiology and neurochemistry of emotions, including love and affection. Neurobiologists have studied pair-bonding Love has been a focus of attention ever since the begin- mechanisms in animal models of mate choice to elucidate ning of mankind, and it has been an important theme for neurochemical mechanisms underlying attachment and artists for thousands of years, being a source of inspiration showed possible roles for oxytocin, vasopressin, and dopa- for poetry, music, literature, paintings, and many other arts mine and their receptors in pair-bonding and monogamy. for as long as they have existed. Recently, romantic love Unresolved is whether these substances are also critically also became a topic of interest for scientists. Love has involved in human attachment. The limited number of avail- able imaging studies on love and affection is hampered by been intensely studied by psychologists and social scien- selection bias on gender, duration of a love affair, and cul- tists in the last century. At the beginning of the last century, tural differences. Brain activity patterns associated with ro- researchers mainly focused on marriage and marital sat- mantic love, shown with fMRI, overlapped with regions ex- isfaction (Berscheid, 2010), reflecting the important posi- pressing oxytocin receptors in the animal models, but defi- tion of marriage in early 20th century society. Romantic nite proof for a role of oxytocin in human attachment is still love was seen as a main factor for “family disorganization,” lacking. There is also evidence for a role of serotonin, corti- sol, nerve growth factor, and testosterone in love and attach- and thus, it should be suppressed to keep stability within ment. Changes in brain activity related to the various stages the family. As research focused on how to keep families of a love affair, gender, and cultural differences are unre- together and prevent marital dissatisfaction, conflict-solv- solved and will probably become important research themes ing studies prevailed, believing that this was the key to a in this field in the near future. In this review we give a resume long and happy marriage. However, these early 20th cen- of the current knowledge of the neurobiology of love and tury investigators might have been wrong because recent attachment and we discuss in brief the truth of human studies indicate that conflict situations within a marriage monogamy. © 2011 IBRO. Published by Elsevier Ltd. All rights reserved. and satisfaction with marriage are two largely unrelated factors. Instead, signs of positive affect (eye contact, cud- Key words: brain activity, romantic love, attachment, hor- dling, positive remarks about each other, etc.) are more mones, gender differences, monogamy. important for marital satisfaction, and absence of positive affect is probably a better predictor of marital problems Contents than conflicts (Huston et al., 2001). Love in an evolutionary perspective 115 During the course of the 20th century, the focus grad- Endocrine factors in love 115 ually shifted from marital satisfaction to romantic love. Oxytocin and vasopressin 115 Dopamine 116 Research on romantic love focussed mainly on why people Serotonin 117 fall in love and how individuals choose a specific partner in Hypothalamic pituitary adrenal axis and cortisol 117 which personality and former relationships are shown to be Nerve growth factor 118 important factors (Berscheid, 2010; Brumbaugh and Fra- Testosterone 118 ley, 2006; Campbell et al., 2005). However, love remained Brain activity in love 119 a research field mainly for psychologists, despite the mas- *Corresponding author. Tel: ϩ31503638790; fax: ϩ31503638875. sive increase in neuroscientific research in the second half E-mail address: [email protected] (G. J. Ter Horst). of the 20th century. This might reflect the common feeling Abbreviations: fMRI, functional magnetic resonance imaging; HPA, hypothalamic pituitary adrenal; NGF, nerve growth factor; OCD, ob- that love is an emotion that cannot be explained by study- sessive-compulsive disorder. ing brain activity and that understanding neuronal corre- 0306-4522/12 $36.00 © 2011 IBRO. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.neuroscience.2011.11.017 114 A. de Boer et al. / Neuroscience 201 (2012) 114–124 115 lates of love will not help us to understand the whole range fourth year of marriage. Based on these data, she devel- of aspects associated with romantic love. However, re- oped her “four-year itch” theory, stating that human adult search has shown that basically every emotion has its pair-bonds are formed for approximately four years, the neuronal correlates, love being no exception. period in which the offspring is most vulnerable. After these In the last few decades, an increasing number of stud- four years, adult pair-bonds can be resolved, allowing both ies has focused on the neuronal correlates of love, unrav- parents to form attachments with other individuals. Thus, eling brain mechanisms involved in the experience of ro- Fisher (1992) suggests that the human mating system is mantic love. Many studies use novel techniques such as one of serial monogamy, not life-long attachments. In fact, functional Magnetic Resonance Imaging (fMRI) and Posi- it much resembles the mating systems found in several tron Emission Tomography (PET) to study the patterns of serial monogamous animals that form pair-bonds for one brain activity of those who are in love. Others study animal breeding season only. The only difference is that the du- behaviors that may be related to human romantic love. ration for the offspring to become independent is much When examining these studies, it is important to keep in longer for humans than for lower mammals. In support of mind that there is an important difference between the Fisher’s theory, she also found that the four years time conclusions based on the biological mechanisms involved window could be extended to about seven years if the in animal pair-bonding and human romantic love in which couple has more than one child, demanding longer coop- psychological mechanisms also play an important role. eration of the parents in the care for the second child. Nevertheless, animal studies on pair-bonding have led to a Romantic love is part of the adult attachment system, rapid increase in knowledge about neural correlates of which is believed to be evolved from an evolutionary much romantic love, although many questions remain unan- older attachment system; mother–infant attachment. At- swered. tachment bonds between mother and infant are most likely In this article, we will integrate and review data from formed around the time of birth. These bonds keep mother psychological studies into the current knowledge of neuro- and infant together for as long as the infant cannot function biological mechanisms underlying romantic love. We ad- independently. Thus, adult attachment and mother–infant dress the evolution of love and attachment, neuroendo- attachment share a functional purpose; both systems crine factors, brain activity, and gender differences in love, evolved to keep two individuals together for a certain pe- and how a love relationship evolves over time. Finally, we riod of their lives (Zeki, 2007). Furthermore, the brain will discuss in brief human monogamy. circuits involved in both attachment systems are largely similar, and oxytocin and vasopressin are the major hor- monal players in both attachment systems. LOVE IN AN EVOLUTIONARY PERSPECTIVE It has been suggested that romantic love developed from ENDOCRINE FACTORS IN LOVE courtship neuronal mechanisms and thus can be seen as a human form of the courtship behavior (Fisher, 1998). Like any other emotion, love is regulated by endocrine Indeed, courtship behavior in lower mammals shares factors. Several factors have been identified as playing a many of the features seen in romantic love, including in- role in romantic love and attachment, including oxytocin, creased energy, focused attention, obsessive following, vasopressin, dopamine, serotonin, cortisol and other affiliative gestures, possessive mate guarding, and moti- stress hormones, nerve growth factor, and testosterone. vation to win a preferred mating partner. Both courtship This chapter will review the role of each of these factors in attraction and romantic love are systems for mate choice, romantic love. evolutionary mechanisms developed to choose a partner Oxytocin and vasopressin that offers the best chances to the offspring. Romantic love is also part of the adult attachment Oxytocin and vasopressin have consistently been impli- system, and it seems to be essential in the early stages of