Pregnancy and parenthood change the brain structure of female mammals. The change makes mothers pay more attention to their offspring and take better care of them
Craig Howard Kinsley and Kelly G. Lambert, Scientific American
Mothers are not born, they are made. All female mammals, from rats, through monkeys, to humans, experience fundamental behavioral changes during pregnancy and motherhood. What used to be an organism directed primarily at itself, devoted to its own needs and survival, became focused on caring for the offspring and caring for its well-being. Scientists have long known about this fascinating change, but only recently are they beginning to understand what causes it. A new study points to the possibility that the sharp hormonal fluctuations that occur during pregnancy, childbirth and breastfeeding cause changes in the structure of the female's brain, such as the increase of neurons in certain areas and structural changes in other areas.
Among the changing areas, some are responsible for maternal behavioral cues such as building a nest, nurturing and cleaning the offspring and protecting them from predators. But they also have areas that control memory, learning and responses to fear and distress. In recent experiments, pregnant rats were more successful at navigating mazes and capturing prey than non-pregnant rats. It is possible that the changes occurring in the brain under the influence of hormones, which motivate the females to take care of their offspring, also improve, in addition to this, the food-gathering skills of the mother rat, and with them the chances of the pups to survive. Moreover, it seems that the cognitive improvement is long-term and accompanies the rats until their old age.
Although the research on the subject has so far only been done in rodents, it is likely that women also derive a lasting benefit from motherhood. In most mammals, the signs of maternal behavior are similar and most likely controlled by the same areas of the brain. Some researchers even claim that the development of maternal behavior was one of the main driving forces in the evolution of the mammalian brain. In the evolutionary transition from reptiles to mammals, the reproductive strategy changed from "lay the eggs and walk away" to "protect the nest", and it is possible that the selective advantages of the second approach led to the formation of the hormonal brain changes and the behavioral signs arising from them. The hand - or the palm - that rocks the cradle indeed rules the world.
are flooded with hormones
About 50 years ago, scientists found the first clues that the hormones secreted during pregnancy fuel the intense emotion that female mammals feel for their offspring. Frank A. Beach of Yale University showed, in research work that began in the 40s, that the female reproductive hormones estrogen and progesterone influence responses such as aggression and sexuality in rats, hamsters, cats and dogs. Further pioneering work by Daniel S. Lerman and Jay S. Rosenblatt, then working at the Animal Behavior Institute at Rutgers University, showed that the same hormones induced maternal behavior in rats. In 1948, Robert S. Bridges, now at the Tufts Cummings School of Veterinary Medicine, reported that the production of estrogen and progesterone increased during pregnancy and that the appearance of maternal behavior depended on interactions between the hormones and their subsequent decline. Bridges and his colleagues went on to show that prolactin, the hormone that causes milk production, stimulated maternal behavior in rats previously treated with progesterone and estrogen.
Besides hormones, there seem to be other chemicals that trigger motherhood by affecting the nervous system. In 1980, Alan R. Gentzler of the State University of New York Medical Center in Brooklyn reported an increase in endorphin levels—pain-relieving proteins produced by the adrenal cortex and hypothalamus region of the brain—during pregnancy in rats, especially before parturition. The endorphins ease the pain during childbirth, but they may also stimulate maternal behavior. Looking at the big picture, it seems that the control of maternal behavior requires coordination between many hormonal and neurochemical systems, and that the female brain is exquisitely adapted to respond to the changes that occur during pregnancy.
Scientists have also identified the areas of the brain responsible for maternal behavior. Michael Numan and Marilyn Numan from Boston College showed that the middle preoptic area in the female brain (mPOA), which is part of the hypothalamus, is largely responsible for this activity; If you create a tumor in the mPOA or inject morphine into the area, the typical behavior of mother rats goes awry. But other brain areas are also involved, and each of these sites contains many receptors for hormones and other neurochemicals. Renowned neuroscientist Paul McLean from the American Institute of Mental Health believed that the neural pathways from the thalamus, which is the relay station of the brain, to the cingulate cortex, which controls emotions, are an important part of the whole of maternal behavior. Damage to the girdle ridge in maternal rats disrupts their maternal behavior. In his 1990 book, The Triune Brain in Evolution, McLean hypothesizes that the formation of these pathways contributed to the shape of the mammalian brain during its evolution from the simpler reptilian brain.
Interestingly, after the stimulation of the initial maternal response by reproductive hormones, the brain's dependence on these hormones apparently decreases, and the offspring alone can stimulate maternal behavior. Although the offspring of a mammal is a small and demanding creature, not really attractive in many respects - it smells, is helpless and sleeps only intermittently - the mother's devotion to taking care of its needs is the strongest drive in animals, even stronger than the one underlying sexual activity and eating. Joanne E. Morrell of Rutgers University suggested that the offspring themselves are the reward that reinforces maternal behavior. When mother rats are given the choice between cocaine and newborn pups, they choose the pups.
Craig Ferris of the University of Massachusetts Medical School recently studied the brains of lactating rats using functional magnetic resonance imaging (fMRI), a non-invasive method that tracks changes in brain activity. Ferris discovered that during breastfeeding there was a marked increase in activity in the nucleus accumbens region of the rat's brain, which is associated with reward and satisfaction. And Ronald J. Gendelman of Rutgers University showed that when a mouse is allowed to press a bar in its cage and get more and more adopted pups sliding in, it will continue to press the bar until the cage is filled with squirming pink creatures.
Some researchers have hypothesized that when nursing puppies latch onto the mother's nipple, they release tiny amounts of endorphins in the mother's body. It is possible that these natural pain relievers act as an addictive drug and draw the mother again and again into contact with her cubs. Sucking and touching the puppies also release the hormone oxytocin, which may have a similar effect on the mother. It could be that inferior species of mammals, such as mice and rats, who obviously do not have high principles and motives like humans, care for their offspring for the simple reason that it makes them feel good.
But what about the motives of the human mother? Jeffrey P. Lorberbaum of the Medical University of South Carolina used fMRI to examine the brains of mothers as they listened to their babies cry. The patterns of activity were similar to those of rodent mothers: the mPOA region of the hypothalamus and the preparietal and prefrontal cortex "lit up". What's more, Andreas Bartels and Samir Zaki from University College London found that brain regions involved in reward control were activated when mothers just watched their children. The similarity between the human response and that of the rodents suggests the existence of a general maternal circuit in the mammalian brain.
brain changes
To understand how this circuit works, the researchers examined the changes in the female's brain during the various stages of reproduction. In the 70s, Marian S. Diamond of the University of California at Berkeley presented early evidence in her research on the cerebral cortex of pregnant rats. The cerebral cortex, which is the outer layer of the brain, receives and processes sensory information and controls voluntary movements. Rats raised in an environment rich in sensory stimuli, surrounded by wheels, toys and tunnels, developed more convoluted cortices than rats that lived in bare cages. But Diamond discovered that the cerebral cortex of pregnant rats raised in a poor environment was just as convoluted and complex as that of females raised in high-stimulus cages. She concluded that a certain combination of hormones and factors related to the fetus gives stimuli to the brains of pregnant rats.
Twenty years later, after studies demonstrated the centrality of the mPOA in maternal behavior, researchers began to look at the changes in this area of the brain. In the mid-90s, Lori Kaiser, a researcher in one of our (Kinsley's) labs at the University of Richmond, showed that the volume of the cell bodies of the neurons in the mPOA of pregnant rats increased. Moreover, the length and number of the dendrites (the branches that branch from the cell body and receive the signals) in the neurons of the mPOA increases as the pregnancy progresses. The same changes were also observed in female rats that received the female hormones progesterone and estradiol at times and in doses that mimic pregnancy. Such changes in neurons are usually accompanied by an increase in protein synthesis and activity. Basically, pregnancy hormones "warm up" the neurons in the mPOA in anticipation of birth and the demands of motherhood. The neurons, like racehorses waiting at the gate, dig in the dirt before they are sent to the track. After birth, the mPOA neurons direct the mother's motivation and attention to her offspring, and this is what allows her to care for them through the variety of behaviors known under the general name "mothering".
However, the maternal behavior has many more aspects than the direct care of the offspring, so we thought that there might be changes in other brain areas as well. For example, the mother rat puts herself at risk to protect the nest and the cubs. She often has to leave the relative safety of the nest to forage, exposing herself and her helpless offspring to predators, because if she stays in the nest she and her cubs will starve to death. We could predict two cognitive changes that would improve the cost-benefit ratio of the mother rat. One, improving her collecting skills, for example, by improving the spatial perception used to navigate the environment. Such an improvement will reduce the duration of her absence from the nest. The second, reducing fear and anxiety will make it easier for her to leave the nest, allow her to gather food faster and prepare her for confrontations in a hostile environment.
In 1999, we found evidence for the first hypothesis when we showed that giving birth to offspring improves the rat's spatial learning and memory. Young females that had been through one or two pregnancies were much more successful than rats of the same age as rats that had not yet dreamed of remembering the location of food rewards in two different types of mazes: an eight-arm radial maze and a terrestrial version of the Morris water maze: a large circular cage with nine food spools. The improved picking skills were observed both in lactating females and in mothers who had weaned their offspring at least two weeks earlier. Moreover, unconceived females that raised adopted pups exhibited the same skills as lactating females. This result shows that the mere presence of the puppies can improve spatial memory, perhaps by stimulating brain activities that change the structure of neurons or by causing the secretion of oxytocin.
Are there also improvements in other characteristics of the mothers' hunting skills? In recent work done by students Naomi Hester, Natalie Karp, and Angela Orthmeier in Kinsley's lab, it was discovered that mother rats were faster at capturing prey than non-pregnant rats. Slightly starved rats were put into cages with an area of about half a square meter, lined with wood shavings, inside which crickets were hidden. Non-pregnant rats took nearly 270 seconds to find and eat a cricket, while lactating females did so in just over 50 seconds. Even when the non-pregnant females were starved more than the mothers, or when the sounds of the crickets were masked, the mothers were able to reach the prey faster.
As for the second suggestion, Inge Neumann of the University of Regensburg in Germany has repeatedly shown that pregnant and lactating rats feel less fear and anxiety (as measured by blood levels of stress hormones) than non-pregnant rats when faced with challenges, such as forced swimming. Jennifer Wortla confirmed these results while working in Kinsley's lab, and extended them by looking at rats placed in a half-square meter cage. She found that mother rats went out more to explore their surroundings and were less likely to freeze in place - two clear signs of courage. We also found a reduction in neural activity in the CA3 region of the hippocampus and the basolateral amygdala, two areas of the brain that control emotion and emotions. The two changes - the moderation of fear responses and the resulting startle, and the improvement in spatial ability - ensure that the mother rat will be able to leave the safe environment of the nest, gather food efficiently and return home quickly to care for the helpless offspring.
Changes in the hippocampus, which controls memory and learning as well as emotions, appear to play a central role in causing these behavioral changes. Fascinating work by Catherine Woolley and Bruce McEwan of Rockefeller University showed ebb and flow patterns in the CA1 region of the hippocampus during the estrous cycle of female rats. The density of dendritic spines—tiny spiny projections that increase the surface area for receiving nerve signals—increased in this region as the female's estrogen levels increased. If the short hormonal fluctuations of the estrous cycle caused such an impressive structural change, we wondered, what would happen to the hippocampus during pregnancy, while estrogen and progesterone levels remain high for an extended period? In Kinsley's lab, Graciela Stafiso-Sandos, Regina Eriner, and Princey Cuadros examined the brains of rats in the last stages of pregnancy, as well as the brains of females treated with pregnancy hormones, and found a higher than normal density of spines in CA1. Since these stingers direct sensory input to the neurons associated with them, it is possible that the significant increase in their density during pregnancy contributes to the mothers' increased ability to navigate mazes and capture prey.
Oxytocin, the hormone that stimulates labor contractions and milk secretion, probably also affects the hippocampus and improves memory and learning. Kazuhito Tomizawa and his colleagues at Okayama University in Japan reported that oxytocin participates in establishing lasting connections between neurons in the hippocampus. Injecting oxytocin into the brains of non-pregnant mice improved their long-term memory, probably by increasing the activity of enzymes that strengthen the connections between neurons. In contrast, injecting oxytocin inhibitors into the brains of maternal rats impaired their ability to handle memory tasks.
Other researchers focused on the effects of motherhood on the connective tissue of the central nervous system called glial cells. Gordon W. Gifford and students in Kinsley's lab studied astrocytes, which are star-shaped glial cells that provide nutrients and structural support to neurons. They found that in late-pregnant, lactating, and hormone-treated rats, astrocytes in the mPOA and hippocampus were significantly more numerous and complex than those in nonpregnant females. Again, hormonal fluctuations seem to amplify neural activity during pregnancy: they change neurons and glial cells in critical brain regions to enhance spatial learning and memory.
Do these cognitive benefits continue to exist even after the breastfeeding period? Work by Jessica D. Gatewood and other students in Kinsley's lab showed that maternal rats as young as two years of age—equivalent to more than 60 years of age in humans—learn spatial tasks more quickly than nonpregnant rats of the same age and show milder memory decline. At each age tested (6, 12, 18 and 24 months), the mothers remembered the location of the food rewards better in the mazes compared to females that did not conceive. And when we examined the brains of the mother rats at the end of the experiment, we found less deposits of pre-amyloid proteins (APP) - which seem to play a role in the degeneration of the aging nervous system - in two areas of the hippocampus, the CA1 and the dentate gyrus.
Jennifer Love, Ilan M. McNamara and Melissa Morgan in another of our labs (Lambert's), recently studied a different strain of rats and under different experimental conditions. This study confirmed that old maternal rats have an enhanced ability of long-term spatial learning. Moreover, the researchers tested the rats' courage using a maze in the shape of a symmetrical cross with two open arms. Rodents tend not to enter such places, which are elevated and exposed and have no hiding places. At most ages tested, up to 22 months, the mothers stayed in the open, fearful arms of the maze longer than the non-pregnant rats. When the mothers' brains were examined, fewer degenerated cells were found in the cingulate ridge in the frontal and parietal cortex - areas that receive significant sensory input. These results suggest that the repeated flooding of the female's brain with pregnancy hormones, along with the rich sensory environment of the nest, may moderate some of the effects of aging on the brain.
The human connection
Are women also getting hired in a similar way from pregnancy and motherhood? Recent studies show that in the human brain there are parallel changes in sensory control systems. Alison Fleming of the University of Toronto in Mississauga has shown that mothers are able to recognize many of their babies' smells and voices, perhaps thanks to enhanced sensory skills. She and her colleagues found that mothers who, immediately after birth, were found to have high levels of the hormone cortisol, showed more attraction and responsiveness to the smell of their babies and were better able to identify crying. The results show that cortisol, whose level usually increases in stressful situations and can be harmful to health, may have a positive effect on new mothers. The strain of parenting may result in a sharpening of attention, vigilance and sensitivity by increasing the cortisol level, thus strengthening the bond between mother and child.
Other studies have suggested that motherhood may have long-term effects. Thomas Perles and his colleagues at Boston University examined people 100 years old and older in New England, USA. Among other things, they found that the chance that women who were pregnant at age 40 or older would live to be 40 years old was four times higher than women whose pregnancies ended at a younger age than that. Perles interpreted the findings as suggesting that the women who conceived naturally after age XNUMX simply aged at a slower rate. But we would add that it is possible that the pregnancy and subsequent motherhood improved the women's brains during the critical period of the beginning of the decline in the level of reproductive hormones. The cognitive benefits of motherhood may have helped delay the loss of memory-protecting hormones, thus contributing to better neural health and longer life.
Could it be that motherhood gives women an advantage in competing with others for limited resources? Unfortunately, there have been almost no studies comparing the learning skills or spatial memory of maternal women with those of non-maternal women. In 1999, a study led by Jay Galen Buckwalter of the University of Southern California showed that pregnant women's success rates on verbal memory tests were below average, but jumped after giving birth. But the study was small (19 women) and did not find significant changes in general intelligence. Journalist Catherine Ellison, in her book The Mommy Brain, describes many cases where the skills required during parenting may help women in the workplace as well. Good leadership requires sensitivity to the needs of employees and constant vigilance for possible challenges and threats. But do these skills successfully transfer from the children's room to the boardroom?
The researchers began to focus on one skill traditionally associated with motherhood: the ability to multitask. Do changes in the maternal brain allow mothers to balance competing demands - child care, work, social obligations, etc. - better than women who are not mothers? Scientists still don't know the answer, but studies suggest that the human brain is extremely plastic: its structure and activity can change when a person is faced with a challenge. Arne May and colleagues at the University of Regensburg found structural changes in the brains of young women and men who learned to juggle three balls in the air. The special areas for perception and prediction of movement expanded after the subjects learned to bounce the balls, and returned and shrank after they stopped practicing. Similarly, it is possible that changes in the mother's brain give the mother the ability to "juggle" between the many and different demands of motherhood.
Animal studies show that mother rats excel at multitasking. In experiments conducted in Lambert's lab, mother rats almost always beat nonpregnant rats in competitions that required parallel tracking of sights, sounds, smells, and other animals. In a race to find a favorite food, rats that had two or more pregnancies reached the food first 60 percent of the time. Rats that gave birth once won the prize 33 percent of the times, and rats that did not give birth - only 7 percent of the time.
And finally, what about the father's mind? Are fathers who take care of their offspring mentally exhausted? Studies of the Brazilian marmoset monkey may provide clues to the answer. The marmoset is monogamous, and both parents participate in the care of the offspring. Ann Garrett from Lambert's lab, in collaboration with V. Jessica Capri and Sean Evans from the Monkey Park in Miami, Florida, tested pairs of marmoset parents on a "picking tree" on which the monkeys had to learn which containers had the most food. The parents - both mothers and fathers - did better in the test than monkeys without offspring. This result confirms studies that examined a species of mice (Peromyscus californicus) in which the male participates to a large extent in the care of the offspring. Erica Glasper and other students in Lambert's lab found that father mice, like mothers, had an advantage in the continental maze. Ashley Everett and Kelly Tu showed that in exploring new stimuli, such as Lego blocks, the fathers were faster than their single friends.
It therefore seems that placing offspring generates changes in the mammalian brain that cause a change in skills and behavior, especially in females. For the female, the greatest challenge from an evolutionary perspective is to ensure that her genetic investment thrives. Maternal behavior evolved to increase the female's chances of success. This does not mean that in every task the mothers are more successful than their friends who did not conceive; Most likely, the improvements only concern behavioral characteristics that affect the survival of the offspring. Still, it seems that adapting the brain to the challenges of motherhood brings with it a lot of benefits. So it can be said: courage turned out sweet.
Mother knows best
Recent experiments show that placement of offspring improves spatial learning and memory in rats and alleviates anxiety and stress. These changes in behavior can improve the foraging skills of mother rats and increase their offspring's chances of survival.
An eight-arm radial maze
First, the researchers let the rats familiarize themselves with a radial maze in which all eight arms contained food baits, then four, then two, and finally only one. So the researchers measured how well the rats remembered in which arm the bait remained. Mother rats with two or more pregnancies were usually able to complete a maze (that is, find the bait within three minutes) already on the first day of the experiment. Females that did not conceive reached a similar success rate after only 7 days.
Overview / Mother's Mind
- Studies in rodents have shown that pregnancy hormones cause changes not only in the areas of the brain that control maternal behavior but also in the areas responsible for memory and learning.
- These changes in the brain may explain why mother rats are more successful in navigating mazes and capturing prey than non-pregnant rats.
- Scientists are now investigating whether motherhood also gives women mental advantages.
About the authors
Craig Howard Kinsley and Kelly J. Lambert studied for more than ten years the
The effects of pregnancy and motherhood on the female brain. Kinsley is a professor of neuroscience in the Department of Psychology and Center for Neuroscience at the University of Richmond in Virginia. Lambert is Professor of Neuroscience and Behavioral Psychology, Chair of the Department of Psychology, and Co-Director of the Office of Undergraduate Student Research at Randolph-Macon College, University of Virginia.
And more on the subject
Mother Nature: Maternal Instincts and How They Shape the Human Species. Sarah B. Hardy. Ballantine Books, 2000.
The Maternal Brain: Neurobiological and Neuroendocrine Adaptation and Disorders in Pregnancy and Postpartum. Edited by JA Russell, AJ Douglas, RJ Windle and CD Ingram. Elsevier, 2001.
A Tribute to Paul MacLean: The Neurobiological Relevance of Social Behavior. Edited by KG Lambert and RT Gerlai. Special issue of Physiology and Behavior, Vol. 79, no. 3; August 2003.
The Neurobiology of Parental Behavior. Michael Numan and Thomas R. Insel. Springer-Verlag, 2003.
The brain savant
