Welcome to the fourth installment of

Mind Matters

Mind Matters is Sciam.com's "seminar blog" on the sciences of mind and brain. Each week, top researchers describe their disciplines' most significant new findings -- and what they, as fellow researchers, find most exciting, maddening, significant, odd, or otherwise noteworthy in the research driving their fields. Blog visitors can participate. We hope you'll join us.

This week we look at two papers on neuronal enrichment:

Experience induces structural and biochemical changes in the adult primate brain

Proceedings of the National Academy of Science 28 November 2005
by Yevgenia Kozorovitskiy, Charles G. Gross,
Catherine Kopil, Lisa Battaglia, Meghan McBreen,
Alexis M. Stranahan, and Elizabeth Gould
Princeton University

Fatherhood affects dendritic spines and vasopressin V1a receptors in the primate prefrontal cortex

Nature Neuroscience 20 August 2006
by Yevgenia Kozorovitskiy, Maria Hughes, Kim Lee & Elizabeth Gould Princeton University




by David Dobbs, Editor, Mind Matters
That the brain responds to life's experiences by changing physically seems at once glaringly obvious and endlessly surprising. How could we possibly adapt to different situations if our brains didn't change? Yet it's easy to find actual descriptions of these changes arresting and almost alarming. Physical alterations you can count or measure -- changes in number and length of dendrites, creation of new neurons -- seem too finite to account for the subtle adjustments in thought, behavior and knowledge we call learning. Thus the fascination of studies like the two discussed here. Both come from the lab of Liz Gould at Princeton, a "powerhouse," as one researcher recently put it, of research on how positive changes in experience or environment ("enrichment," in the neurojargon) affect the brain. (For a good profile of Gould and her work, see this article by Jonah Lehrer.) One shows that the neuronal benefits of enriched lab environments, found many times in rodents, occur in marmosets as well -- a finding unsurprising, given the rodent record, but significant for extending the finding to primates and thus a bit closer to our human home, as it were. The other paper shows that fatherhood creates similar brain changes in marmoset. That finding is new -- and to addled parents too tired to think, a bit surprising. Both papers carry interesting implications. Here to explore them are psychologists Julie A. Markham of the University of Ililnois and Martha J. Farah of the University of Pennsylvania. Join them, and us, in an enriching discussion.

How is Fatherhood Like a Better Room?

by Julie A. Markham

Fatherhood affects dendritic spines and vasopression V1a receptors in the primate prefrontal cortex," the first study to describe fatherhood's effects on the primate brain, compared the brains of marmoset fathers actively participating in infant-rearing with those of adult male marmosets who were not fathers. Rather than looking at a brain region known to be directly involved in parenting behavior, such as the hypothalamus (an area situated at the base of the brain that regulates many basic survival behaviors), Kozorovitskiy and colleagues did something more interesting: they looked for changes in the prefrontal cortex, an area involved in the highest-order cognitive processes, such as working memory and the organization of behavior. They found that fatherhood causes neurons in the prefrontal cortex to form many new dendritic spines. These small protuberances stud a neuron's dendrites, which are extensions that receive signals sent across synapses by other cells. This is a stunning finding. Prefrontal cortical neurons are some of the most complex in the nervous system. And as Guy Elston's work suggests, in primates a positive relationship exists between the complexity of prefrontal neurons and intelligence. That fatherhood increases dendritic spines on prefrontal neurons -- which likely increases communication between them -- is tremendously intriguing. Not Just Hormones The idea -- or at least the proof -- that raising young could be good for the brain was virtually unheard of until 1999. That is when Craig Kinsley and colleagues reported that female rats experienced in raising pups -- whether or not they had ever been pregnant -- outperformed females who had not raised pups on certain memory tests. Subsequent studies showed that motherhood increased dendritic spines on neurons in the hippocampus, a region important to forming memories. Both the cognitive benefits of motherhood and the enrichment effects were relatively permanent, extending into old age. Until this paper, however, no one had studied how fatherhood remodels the prefrontal cortex in any species, and no one had studied how fatherhood affects the brain in primates. Although fatherhood brings hormonal changes, those hormonal changes probably only partly explain the changes in brain morphology observed by Gould's group. While changes in the brain (including those induced by hormones) undoubtedly alter behavior, the relationship is bidirectional -- engaging in certain behaviors can have dramatic effects on brain structure. Mark Rosenzweig and colleagues first reported in the 1960s that rats raised in a complex environment -- a large cage filled with toys and other objects -- possessed heavier and thicker cerebral cortices than did rats raised in standard lab conditions. The rats in bigger, more complex and stimulating environments were already known to do better on tests of rodent cognition; the Rosenzweig study helped explain why. Subsequent work demonstrated that the thicker cortex was due to the growth of neurons, and was accompanied by increases in the number of dendritic spines on those neurons. Since then, the work of Bill Greenough and others has shown that the neural consequences of such "enriching" experiences are related specifically to active engagement in behaviors that promote learning, and not to general increases in physical activity or hormones. These neural changes are relatively permanent, lasting well beyond the enriching experience. Later studies, including the 2005 paper from the Gould lab considered here, "Experience induces structural and biochemical changes in the adult primate brain," showed that more complex environments spurred neuronal growth in primates as well. In that study, Kozorovitskiy and colleagues compared marmosets housed in a complex habitat to those living in a standard cage. They found effects similar to those they later observed as a consequence of fatherhood: dendritic spines increased on neurons in the prefrontal cortex, as did the overall size of these neurons. So how does fatherhood create these changes? Gould's group found that fatherhood increased the number of receptors in the prefrontal cortex for arginine vasopressin, a peptide hormone involved in the formation of social bonds. They propose that the resulting increase in vasopressin signaling could have caused the increases in dendritic spines. Their previous enrichment work, meanwhile, indicates that behavioral changes that go with fatherhood could also contribute to the observed spine changes. Interestingly, they provide evidence that the abundance of vasopressin receptors was reduced over time as infants aged -- suggesting that this particular change is temporary and driven by recent contact with infants. A comparable examination of whether the spines also tended to decrease over time, in parallel with the reduction in vasopressin receptors, would have been informative. If the increases in dendritic spines demonstrated more permanence, the case for the experience of fatherhood as a form of enrichment would be strengthened. What Triggers a Father to Start Acting Fatherly? In reading this article, I wondered what could be signaling the initiation of paternal behavior in these animals in the first place. Women can simply announce to their partners, "Honey, I'm pregnant!" But what tells a male marmoset that his mate is expecting? (We know that they know, because as in humans, hormonal changes are observed in expectant marmoset fathers.) Though these primates do not benefit from linguistic communication, they still manage to gear themselves up for infant care, which suggests that other factors may also be at work in our own species. This study was not designed to address this question. A little digging into the scientific literature, however, reveals that, in rodents as well as marmosets, paternal responsiveness to infants relies partly on the strength of the breeding pair's relationship prior to the offspring's birth. This has profound implications for human fathers: Creating a strong bond between father and partner before starting a family could make for better dads. And, as this paper suggests, taking an active role in parenting can be enriching for the father's brain as well as the children's. The next logical step in this line of research will be to see whether all these brain changes actually make dads smarter. We've already seen that female rats who raise pups do better on memory tests. Do fatherhood-induced changes in the primate prefrontal cortex improve higher cognition? A finding like that could inspire a guy to push a stroller.

Julie A. Markham is a postdoctural fellow in the William T. Greenough Laboratory at the Beckman Institute, a neuroscientific research institute at the University of Illinois at Champaign-Urbana. She and Greenough recently coauthored the review article "Experience-driven brain plasticity: beyond the synapse."


Enriched Environments in Humans:
Can You Study That?

by Martha J. Farah

As a cognitive neuroscientist working with human subjects, I envy the ability to carry out experiments on how environment changes brain function. Don't misunderstand me -- human cognitive neuroscience includes plenty of good experimental designs, and we can generate testable hypotheses and critical experiments with the best of them. But ethical considerations prevent us from confining our subjects to isolated and barren chambers or, for that matter, forcing fatherhood on them. We can, however, make scientific use of naturally occurring differences in people's environments. We can't assign some people to impoverished environments and others to enriched ones, but we can find people who happen already to be living in such environments. Compared with people of higher socioeconomic status, people of low socioeconomic status, for example, tend to inhabit smaller homes than most people and have fewer possessions, fewer opportunities for hobbies, sports and other diversions, and less stimulating jobs. One could measure aspects of their brain function and see whether these environmental differences correlate with brain differences. Confounding Factors Astute readers will recognize a problem with this strategy: socioeconomic status is correlated with more than just a certain level of environmental enrichment, and some of these other correlates -- for example, physical health status -- might create any observed differences in brain function. However, this problem can be minimized (though never entirely eliminated) by measuring as many of the potential confounds as possible and including them in one's statistical analysis. We have taken this strategy in my lab, and as we reported last year, we have found that, at least for children, poverty is associated with differences in hippocampal memory function and prefrontal executive function (as well as language ability, which for obvious reasons Kozorovitskiy and colleagues did not assess) in ways that agree strikingly with the findings in Kozorovistkiy's study on enriched environments. There is another way to test the effect of environmental enrichment on human brain function as well -- one that amounts to a nicer version of assigning people to impoverished and enriched environments. Instead, we begin with people from equivalently impoverished environments and randomly assign some to improved, more enriched environments. A number of early childhood intervention programs for poor families have provided just this experimental manipulation and have shown substantial and lasting results (see, for example, the Abecedarian project). The measures that have been used so far to demonstrate these program's psychological impacts are difficult to map onto the functioning of specific brain systems. But more direct neural measurements could in principle be taken. Science and Society Such research would have two very important kinds of implications. The first is for science. The human brain is distinctive in the diversity of ways in which it interacts with its environment: understanding its physical surroundings, engineering them, decorating them, and engaging with other individuals and groups both verbally and nonverbally. The relationship between brain and environment is therefore a central issue for human cognitive neuroscience. Evidence from animal experimentation provides an excellent foundation, but only a foundation, for research on how environment influences human brain function. The second implication is for society. If the type of environment we're in can enhance or diminish our brain function, and if socioeconomic factors confine some of us to environments that literally damage our brains, then poverty is more than a problem of economics. It is a problem of public health, directly affecting the biological substrate of who we are and what we can become. Perhaps by understanding the problem in these terms we can find the political will to improve the limited, stressful, and generally hopeless situations to which the poor in our society are confined.

Martha J. Farah is the director of the Center for Cognitive Neuroscience at the University of Pennsylvania. With degrees in metallurgy and materials science, philosophy and experimental psychology, she brings a range of perspectives to her work on cognition, psychology and behavior. She has researched and written widely on the mechanisms of memory, vision, and executive function. More recently she has examining the interface between cognitive neuroscience and the "real world," particularly the impact of socioeconomic adversity on brain development and emerging social and ethical issues within neuroscience.