How unpredictability in food-related environments influences social relationships and behavior stability
Date: Thursday, May 11th, 2000
Title: “Individual Patterns of Fluid Ingestion within Monkey Social Groups”
Speaker: Leonard A. Rosenblum, Ph.D., State University of New York Health Science Center at Brooklyn
Unpredictability in food-related environments alters maternal primate social relationships and behaviors, as well as the long term neuronal and social development of their offspring. Such alternations are independent of nutritional status and seem directly related to stress induced by an unpredictable foraging environment. When inconsistent foraging requirements are placed on a maternal primate during the first 6 months of her offspring’s life, her maternalistic behaviors change, and her offspring’s behavioral and neural development suffer.
Inconsistent foraging requirements are generated by alternating the effort exerted (which is defined as the amount of time and complexity required to access food) by the mother in order to obtain access to daily nutritional needs. In the series of studies reviewed, foraging requirements were alternated bi?weekly between difficult and easy levels of effort to access daily rations in a group of gregarious primates, the Bonnet Macaques. This alternating paradigm is referred to as “variable foraging demand” (VFD). The general experimental design that was employed for these studies included three groups of mother?infant pairs: a consistently high foraging demand group, in which the mothers had to dig through wood-chip bedding in order to obtain food; a consistently low foraging demand group, in which food was simply available on the floor of the pen; and a variable foraging demand group, which alternated between the two conditions in two-week blocks during the 12 weeks of the study. The foraging experiments generally began when the infants reached 8 weeks of age. In addition to the wood?chip foraging, in related studies, foraging demand has also been induced by placing food inside panels of shelves and drawers; the animal would have to put her hand into each drawer until she found some food. Regardless of the mode of foraging employed, the level (high or low) and variability (alternating) in foraging demand seemed to be the critical variable in predicting subsequent behavioral and developmental disturbances. Primates in all groups received full daily rations of food, so nutritional status was not a factor in the differences in development between the groups. In some studies, to further ensure that nutrient demands were met, the infants had access to food and water in a separate area not accessible to the mothers.
In any high foraging situation, the primates learned techniques in order to remember where food had been previously, and how they could systematically search for rations. In studies in which stacks of sites (e.g. drawers) were used, the animals learned to take food from smaller panels first, rather than bigger panels, and they would take from the periphery of the panels and work their way inward. This type of organization indicated that the animals achieved a location?learning effect. The level of foraging demand also apparently increased the value of food, such that when animals were placed under a high-demand condition they tended to consume every last item, but for low?demand conditions, they would leave extras. In keeping with the work of Collier, these data suggest that food preferences are less pronounced when subjects are required to work harder or longer to obtain each food item.
Both during and after the foraging schedule, several differences between the behaviors of both the infants and mothers who had been living under VFD conditions emerged. The infants showed evidence of anxiety?related behaviors, depending on the stage of development. For instance, VFD?reared primates clung to their mothers, whereas predictably-reared monkeys were apt to leave their mothers and explore a novel environment. Older VFD?reared primates exhibited social timidity by huddling less than primates raised in the control group. The inconsistent, erratic, and sometimes dismissive rearing behavior exhibited by mothers undergoing variable demand foraging is the putative mechanism that eventually diminished the infants’ perception of a ‘security’ of maternal attachment.
Subsequent studies of these animals in adulthood revealed that the function of neuronal systems concerned with stress modulation appeared permanently altered by the VFD paradigm. In particular, cerebrospinal fluid (CSF) concentrations of corticotropin-releasing factor (CRF) were normal in both the high demand and low demand primate groups, but monkeys raised under the variable foraging conditions showed an increase in CRF levels. Other neurochemical markers of anxiety disturbances in the VFD primates included exaggerated behavioral response to noradrenergic stimulation, blunted behavioral response to serotonergic agonists, and blunted growth hormone response to a clonidine treatment. Thus, even years after a relatively subtle disruption of maternal?infant interaction, animals whose mothers underwent an uncertain variable foraging demand condition are fearful and shy and show evidence of enduring biological disruption. These results are particularly interesting because there are similar neurochemical correlates of stress in people with post-traumatic stress disorder, such as Vietnam veterans.
As an extension of the foraging studies, measures of consummatory behavior and task performance are being analyzed. To study task performance, primates are offered access to video games which vary in complexity. The primates play the games within their typically large, free?moving social groups. The video game paradigm is being used to test the effects of various psychopharmacological agents on task performance and on social interaction. Through the use of electronic chips implanted in the monkeys’ wrists, computers can monitor both the details of individual fluid consumption and game playing in free-moving social groups. Ethanol, methamphetamine, and yohimbine have all been studied. Results of studies on patterns ethanol consumption revealed that, as with humans, there are tremendous individual variations in preferences and quantities desired. The video game is a sensitive measure for assessing drug effects since administration of a relatively low dose of yohimbine, an anxiogenic agent, diminished interest in the food rewarded games, but only if the video game was not set to a high level of complexity. In social groups, the number of errors increased as the monkeys consumed more ethanol. Much more work is underway to study how these drugs influence the primate social interactions and cognitive performance.
In summary, these studies with primates show that unpredictable environments can lead to life?long disruptions in emotional stability. It is as yet unclear whether the permanent disturbances result from a transference of stress from the caretaker onto the infant, or if the infant directly experiences some sort of anxiety which becomes reinforced throughout development, under these circumstances.
Kissileff: So is this a primate model of a working mother?
A: Very much so, because the males only contribute to the perpetuation of the species!
Collier: Would you then also consider the VFD regimen analogous to our current ‘boom and bust’ economic environment?
A: There certainly are correlates. For example, in other primate studies of unpredictable lifestyles, ulcers developed, just like they do in humans. There is clearly an importance in primates, including humans, to have a level of predictability in their lives. Even in the case of reward paradigms, the variable?reward schedule seems the strongest. It is important to note here that the VFD schedule is only influential when implemented during the first few months of life (less than 6 months of age), which has been shown to be the most critical period of synaptic development. The take home message in this work is undoubtably that stability is critical during early years of life, and that seems to hold true from monkeys to humans. What is less critical is how much you have? just that you know what you have!
Nolan: Did the monkeys engage in any bizarre, food?related behaviors? such as hoarding? once they were put back on a schedule?
A: Actually that was not studied but sounds like an interesting question to pursue.