Long-term attachment, which includes pair bonding with a sexual partner and parental bonding with offspring, are naturally rewarding behaviors in some species of mammals.
Much of the research on social attachment and mammalian pair bonding has been done using voles as the animal model. Voles are useful because there are closely related species that display considerably different reproductive behavior. The prairie vole (Microtus ochrogaster) that is indigenous to central North America is an atypical rodent that displays highly social behavior, has monogamous relationships after mating, and will cohabitate and share parental duties such as mutual resource collections, nest building, and care for their young. The montane vole, on the other hand, has a slightly different geographical location and is a non-social species. They do not form pair bonds and only the female cares for the young.
An experimental test called the partner preference paradigm can be used to assess vole monogamy. Here, a three-chamber testing apparatus is used where a test vole is placed in a central chamber. In the other two chambers are voles who have been harnessed into their rooms, unable to leave. The test vole is then free to move between any of the three chambers. When a prairie vole has mated with one of the harnessed voles, they will choose to spend more time with their “partner” vole compared to the novel “stranger” vole, whereas a montane vole will choose to spend most of their time alone and spend very little time with any other animal. Differences in brain and behavior can be studied between these species to determine why they display these different reproductive behaviors.
Not only do mated prairie voles prefer the company of their partner, they also demonstrate behaviors similar to some human romantic relationships. For example, mated prairie voles living together display selective aggression against a stranger, “intruder” voles, a behavior called “mate-guarding”. They also spend significant time mutually caring for their young, their pair bonding can be modified by psychoactive substance use, and they show increased anxiety when they are separated from their partner vole.
Role of Oxytocin and Vasopressin in Pair Bonding
Comparing between monogamous and promiscuous species has allowed researchers to identify several neurotransmitter signals that are implicated in pair bonding. Oxytocin and vasopressin seem to play important roles in vole pair bonding, as inhibition of either of these signals decrease partner preference. Additionally, differences in dopamine receptor levels and corticotropin releasing factors are observed between vole species.
The hypothalamus is a critical region for the formation of social bonds. , the larger type of neurosecretory cell compared to parvocellular neurons, send axons from the hypothalamus down to pituitary stalk where they terminate on capillaries of the general circulation located within the posterior pituitary. Therefore, unlike the control of stress and gonadal hormones, where the hypothalamic neurons release hormones onto anterior pituitary endocrine cells, release of hormones from the posterior pituitary comes directly from hypothalamic neurons.
The magnocellular neurons synthesize and release oxytocin and vasopressin, two neuropeptides, into the blood. Oxytocin, often referred to as the love hormone, promotes social bonding. It is released during reproduction and also causes uterine contractions during labor and the milk letdown reflex after birth. Vasopressin, also called antidiuretic hormone, plays a role in regulating salt concentration in the blood by acting on the kidneys to promote water retention and decrease urine production. Further, it constricts blood vessels, raising blood pressure. Vasopressin has also been shown to be involved in bonding, parenting, territoriality, and mate-guarding in some animals. Biochemically, vasopressin is very similar to oxytocin, as they are both nine amino acid peptides differing by only two residues.
In the social prairie voles, oxytocin and vasopressin are released by the hypothalamus in response to mating and act on regions of the reward and limbic systems. Specifically, there are increases in oxytocin release in female prairie voles following mating. Female prairie voles express higher levels of oxytocin receptors in the nucleus accumbens compared to montane voles. Oxytocin binding to oxytocin receptors within the nucleus accumbens is necessary for females to form pair bonds and may reinforce the association of reward with a partner. This is supported by experimental evidence that when oxytocin is administered to females, there is an increase in pair bond formation. Female montane voles have decreased oxytocin receptors within the nucleus accumbens, and thus do not form pair bonds. Oxytocin does not have the same effects in male prairie voles.
Male prairie voles have an increase in vasopressin release following mating. The male prairie voles express higher levels of vasopressin receptors in the ventral pallidum compared to montane voles. When vasopressin is given to males, it increases pair bond formation, and when a vasopressin antagonist is administered prior to mating, pair bond formation is prevented. Vasopressin has no effect on female prairie voles. The nucleus accumbens and ventral pallidum are both located in the basal ganglia and are involved in the limbic loop, which is responsible for processing of emotions, rewards, and motivation.
An interesting experiment was done that overexpressed vasopressin receptors in the ventral pallidum of male montane voles. The simple manipulation of this one protein completely changed the behavior of the monogamous montane voles such that they now behaved like prairie voles by forming pair bonds and helping to take care of young.
Oxytocin, vasopressin, and the reward system also appear to be important for bonding in humans. When presented with pictures of either their own children or partners, subjects in an fMRI show increased activation in regions like the ventral tegmental area and striatum compared to when viewing pictures of friends. These regions are also known to express oxytocin and vasopressin receptors, and the hormones are released during times of bond formation, like breastfeeding and intercourse.
Love can be thought of as an intensely strong attachment towards a person (romantic love, lust), a thing (passion project), or concept (patriotism as a love for country, or altruism as a love for fellow humans). However, it is very difficult to put a strict biological definition on these varied concepts of love. This section focuses on interpersonal love, of which there are several unique forms, each resulting in different behavioral outcomes. For example, romantic love drives physical attraction, lust, and sexual activity. Parental love, on the other hand, encourages self-sacrifice and hyper-attentiveness towards a newborn. Some behaviors are shared between the two forms of love, such as respect.
Romantic love drives much of human behavior and has been documented thoroughly in the arts all the way from Homer’s Iliad, through Shakespeare’s Romeo and Juliet, up to modern Taylor Swift.
The majority of human societies have embraced social monogamy, the romantic relationship characterized by a pair of people who share resources, parenting duties, and exhibit preferential mating. Outside of humans however, only 9% of mammalian species form socially monogamous pairs, while at least 75% of bird species maintain socially monogamous relationships (which may explain the origin of the phrase “love birds”).
Dr. Helen Fisher, an anthropologist and a leader in the field of love research, suggests that love can be divided into three closely interconnected components. These three are guided in part by different signaling pathways, and lead to somewhat different behavioral outcomes.
Lust (or libido) refers to a very strong desire for sexual gratification. These behaviors are largely driven by the actions of the sex hormones testosterone, estradiol, and progesterone, released downstream of activation of the HPG axis. Both testosterone and estradiol contribute to sex-seeking behaviors in men and women, where increasing testosterone levels drive up sexual desire. The amygdala also plays a significant role in mediating lust, and lesions may either result in hypersexuality (Kluver-Bucy syndrome) or a decrease in response to socially-derived sex cues.
Attraction is characterized by high energy-investment and preoccupation towards a small number of people. From an evolutionary perspective, attraction may have developed to discriminate between multiple reproductive partners, allowing the focusing of limited resources towards fewer partners. In Fisher’s theory, attraction is strongly related to the action of dopamine and norepinephrine. In humans, the reward circuitry is involved in feelings of love. Using fMRI, Fisher presented pictures of a patient’s romantic partner to them and identified increases in the blood flow to dopaminergic midbrain areas such as the ventral tegmental area and the striatum. This finding compares with imaging studies that observed increases in blood flow to insula, premotor, and hypothalamus as well as striatum in response to highly erotic, sexual imagery. These studies suggest that romantic love and lust have different driving neural structures underlying these behaviors. Norepinephrine functions to increase attention, alertness, and energy, which accounts for the exhilarated feeling you may feel when spending time with a potential partner.
Attachment is the long-term association with an individual accompanied by feelings of comfort and emotional stability. Attachment also contributes to behaviors that maximize offspring survivability, such as sharing parenthood responsibilities and protectiveness towards offspring. The major neurochemical drivers of this form of love are oxytocin and vasopressin.
Parental love refers to instinctive affection towards one’s offspring. Parental love behaviors include nurturing (collecting and sharing resources), protecting (promoting aggression against “intruders”), and preparing one’s young for their adult life (risk assessment training). In evolutionary theory, parental love serves to improve the odds of passing of one’s genes through the following generation. Most large mammals (humans included) are K-selected species, which benefit most from a small number of high-quality offspring that require substantial parental investment, as opposed to large numbers of offspring with little investment.
An extension of parental love is familial love or kinship, the protection and preferential support of one’s extended genetic relations. Because blood relatives share common genes, increasing the survivability of these family members has benefits for passing genes to the next generation. In the words of the geneticist Jack Haldane, “I’d gladly give my life for two brothers or eight cousins.”
Many behaviors related to mammalian motherhood are accompanied by changes in neural activity. Nursing, for instance, is feeding behavior that is regulated through a positive feedback cycle. Offspring suckling activates the mother’s somatosensory afferents. Through a series of oxytocin-dependent circuits across the hypothalamus, suckling ultimately increases lactation through the milk letdown reflex. Auditory sensory inputs, such as the sounds of a crying baby, can also trigger this reflex. Sometimes, just thinking about the baby can induce letdown. Some changes are dependent on neural plasticity. For example, after childbirth, the auditory areas of rodents rewire to become more sensitive to high frequency sounds. This adaptation allows the mothers to better detect the ultrasonic vocalizations that are emitted by offspring when they are distressed or hungry. Olfactory areas also change in order to become more sensitive to the particular odorants given off by their young, allowing them to better identify their offspring. In humans, these olfactory changes result in decreased aversion towards traditionally aversive stimuli (urine or fecal matter) when they originate from their children.
- Prairie voles are a socially monogamous species that forms pair bonds with their mating partners and display biparental care of young.
- Montane voles are a closely related species that display a promiscuous mating strategy, do not form pair bonds, and do not show biparental care of young.
- Female prairie voles have increased oxytocin receptors within the nucleus accumbens compared to montane voles.
- Male prairie voles have increased vasopressin receptors within the ventral pallidum compared to montane voles.
- Oxytocin and vasopressin are both neuropeptides released from the posterior pituitary.
- Human bonding and love (romantic and parental) has also been shown to involve oxytocin, vasopressin, and reward circuitry.
Portions of this chapter were remixed and revised from the following sources:
- Foundations of Neuroscience by Casey Henley. The original work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License
- Open Neuroscience Initiative by Austin Lim. The original work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
- Prairie Vole © Davi adapted by Valerie Hedges is licensed under a CC BY-SA (Attribution ShareAlike) license
- VolePreference © Casey Henley is licensed under a CC BY-NC-SA (Attribution NonCommercial ShareAlike) license
- PosteriorPituitary © Casey Henley is licensed under a CC BY-NC-SA (Attribution NonCommercial ShareAlike) license
- OxytocinVasopressin © Casey Henley is licensed under a CC BY-NC-SA (Attribution NonCommercial ShareAlike) license
hypothalamic neurosecretory cells that send axons from the hypothalamus down the pituitary stalk and terminate within the posterior pituitary