Evolutionary developmental psychology: Contributions from comparative research with nonhuman primates

Evolutionary developmental psychology is a discipline that has the potential to integrate conceptual approaches to the study of behavioral development derived from psychology and biology as well as empirical data from humans and animals. Comparative research with animals, and especially with nonhuman primates, can provide evidence of adaptation in human psychological and behavioral traits by highlighting possible analogies (i.e., similar function, but independent evolution) or homologies (i.e., inheritance from a common ancestor) between human traits and similar traits present in animals. Data from nonhuman primates have played a crucial role in our understanding of infant attachment to the caregiver as a developmental adaptation for survival. Primate and human data are also consistent in suggesting that female interest in infants during the juvenile years may be a developmental adaptation for reproduction that facilitates the acquisition of maternal skills prior to the onset of reproduction.     

Cholesterol and aggression

Best known for its etiological influence in the cardiovascular disease process, serum cholesterol also plays a role in numerous psychological processes, including affect, cognition, and overt behavior. Prominently, it is related to aggression in humans and other primates. Lipid studies of violent offenders, primary prevention trials of cholesterol reduction, and experimental dietary manipulations in nonhuman primates all point to a significant negative association between cholesterol and physical aggression. By contrast, a positive though inconsistent association between serum cholesterol elevations and verbal aggression (e.g., hostility) has been reported in many studies and often ascribed to a neurophysiological response to acute or chronic stress. We review the numerous studies that have examined the link between serum cholesterol, verbal and physical aggression, and integrate current findings.     

Scratching as a behavioral index of anxiety in macaque mothers.

The aim of this study was to assess the validity of the notion that anxiety influences maternal style in monkeys. To this end, we investigated the correlations between measures of the quality of mother-infant relationship and scratching, a behavior pattern that reflects a state of anxiety. The subjects were seven group-living macaque mothers and their infants observed during the first 12 weeks postpartum. Postpartum scratching by the mothers was positively correlated with both maternal possessiveness and maternal warmth, two composite measures of the quality of mother-infant relationship that reflect a possessive and attentive maternal style. Evaluation of the correlations between maternal rank and scratching before and after parturition indicated that interactions with their infants, not those with other group companions, were the main source of anxiety for the mothers. These results support the notion that anxiety influences maternal style in monkeys and suggest that studies aimed at investigating physiological and social correlates of maternal emotionality in nonhuman primates could use scratching as a useful and simple behavioral measure.     

Observing conspecifics scratching induces a contagion of scratching in Japanese monkeys (Macaca fuscata)

Although a large number of studies have examined self-directed behaviors (SDBs) such as scratching and self-grooming as nonverbal leakage of negative emotional arousal in humans, few studies have investigated the informative function of SDBs in nonhuman primates. The present study investigated whether viewing another monkey scratching itself elicited negative arousal from conspecific observers in Japanese monkeys (Macaca fuscata). An experimental situation was created in which the target monkey watched a stranger through a small peephole and the observer monkey(s) watched the target in turn. Scratching spread when conspecific observers watched the target scratching itself while performing monitoring behavior. The author proposes that the possible contagion of scratching by monkeys observing another's scratching may involve transmission of a psychological state, a primitive style of empathy.     

Behavioral and physiological correlates of stress related to examination performance in college chemistry students

This study was designed to assess physiological and behavioral correlates of academic stress during a college course in organic chemistry in the USA. Participants (45 females, 46 males, mean age 19.88 years) were screened for their basal hypothalamic-pituitary-adrenocortical activity using saliva samples collected at the beginning of the course and after each major test. Displacement activities (DAs) were observed during each test by videotaping students' behavior when they were taking the tests. These variables were then used as predictors of the students' achievement as measured by their grade point average (GPA) scores, American College Testing (ACT) scores, and their final grade in the class. Ninety-one students, enrolled in Organic Chemistry I at Marshall University during the summer of 2009, were recruited for this study. It was found that individual differences in the physiological stress responses are a factor in predicting the students' ability to pass a challenging class. A logistic model built on GPA, DAs during stress, and salivary hormone (cortisol and dehydroepiandrosterone) concentrations was able to correctly classify almost 90% of the students passing the class. The same model was not nearly as successful in determining the possible factors behind failing the class, because the classification success was just 52%, a figure close to chance. We conclude that a clear set of characteristics related to the students' ability and resilience to psychological stress are necessary to succeed in a challenging class. The reason behind dropping or failing a class could be less defined. These data indicated that investigating the physiological and behavioral propensities associated with psychological stress can help us better understand an individual's coping responses to a long-term challenging situation.     

A review of domestic dogs' (Canis familiaris) human-like behaviors: or why behavior analysts should stop worrying and love their dogs

Dogs likely were the first animals to be domesticated and as such have shared a common environment with humans for over ten thousand years. Only recently, however, has this species' behavior been subject to scientific scrutiny. Most of this work has been inspired by research in human cognitive psychology and suggests that in many ways dogs are more human-like than any other species, including nonhuman primates. Behavior analysts should add their expertise to the study of dog behavior, both to add objective behavioral analyses of experimental data and to effectively integrate this new knowledge into applied work with dogs.     

Disposition to recognize goals in infant chimpanzees

Do nonhuman primates attribute goals to others? Traditional studies with chimpanzees provide equivocal evidence for “mind reading” in nonhuman primates. Here we adopt looking time, a methodology commonly used with human infants to test infant chimpanzees. In this experiment, four infant chimpanzees saw computer-generated stimuli that mimicked a goal-directed behavior. The baby chimps performed as well as human infants, namely, they were sensitive to the trajectories of the objects, thus suggesting that chimpanzees may be endowed with a disposition to understand goal-directed behaviors. The theoretical implications of these results are discussed.     

Benefit Finding and Physical Health: Positive Psychological Changes and Enhanced Allostasis

Many individuals who undergo stressful life events report that they have derived some positive benefit from the experience. Although the majority of research on benefit finding has focused on its psychological correlates, there is intriguing evidence that benefit finding may also have effects on physical health. In this paper, we review the emerging literature on benefit finding and physical health and present an integrative model in which we identify specific psychological and physiological pathways through which benefit finding may influence physical health outcomes. In particular, we consider the hypothesis that benefit finding may involve changes in a number of psychological domains – namely, changes in appraisal and coping processes, relationships, goals and priorities, and positive affect – that lead to a state of enhanced allostasis, buffering against negative effects of catabolic stress responses and promoting activity in restorative physiological systems. Empirical evidence for this model is reviewed, focusing on studies that have examined positive psychological constructs relevant to benefit finding and their effects on stress reactivity, recovery, and habituation, as well as restorative processes.     

IN PURSUIT OF GENERAL BEHAVIORAL RELATIONS

Efforts to develop behavioral technologies from advances in basic research assume that results from studies with nonhuman subjects can, in some instances, be applied to human behavior. The behavioral principles likely to be most useful for application are those that represent robust general behavioral relations. Basic and applied research on behavioral momentum suggests that there is a general behavioral relation between the persistence of behavior and the rate of reinforcement obtained in a given situation. Understanding the factors that affect behavioral persistence may have important implications for applied behavior analysts that justify studies aimed at establishing the generality and limits of the functional relation between reinforcement rate and behavioral persistence. Strategies for establishing the generality of behavioral relations are reviewed, followed by a brief summary of the evidence for the generality of behavioral momentum.     

Biological specializations for speech: what can the animals tell us?

Language research over the past 40 years converges on the speech-is-special hypothesis (SiS), according to which speech perception and production are uniquely human adaptations. SiS is grounded in a variety of biological, developmental, and behavioral evidence. In some comparative studies, speechlike stimuli have seemed to cause nonhuman animals to exhibit humanlike performance functions. Auditorists—who believe that spoken language processing is executed by, and is explicable in terms of, general auditory mechanisms—have seized upon such studies as evidence that SiS is incorrect. However, it is difficult to identify biological and functional similarities across different species on the basis of behavior alone, and the elaborate training regimen that nonhuman animals require to achieve human performance levels undermines the significance of certain comparative studies. Both comparative and human behavioral research, including brain-imaging studies of functional localization, electrophysiological recordings of the neural basis of the perception-production link, and developmental studies of a time-locked schedule of language learning, favor SiS over auditorism.     

Harms and deprivation of benefits for nonhuman primates in research

The risks of harm to nonhuman primates, and the absence of benefits for them, are critically important to decisions about nonhuman primate research. Current guidelines for review and practice tend to be permissive for nonhuman primate research as long as minimal welfare requirements are fulfilled and human medical advances are anticipated. This situation is substantially different from human research, in which risks of harms to the individual subject are typically reduced to the extent feasible. A risk threshold is needed for the justification of research on nonhuman primates, comparable to the way risk thresholds are set for vulnerable human subjects who cannot provide informed consent. Much of the laboratory research conducted today has inadequate standards, leading to common physical, psychological, and social harms.     

Fetal Testosterone Predicts Sexually Differentiated Childhood Behavior in Girls and in Boys

ABSTRACT— Mammals, including humans, show sex differences in juvenile play behavior. In rodents and nonhuman primates, these behavioral sex differences result, in part, from sex differences in androgens during early development. Girls exposed to high levels of androgen prenatally, because of the genetic disorder congenital adrenal hyperplasia, show increased male-typical play, suggesting similar hormonal influences on human development, at least in females. Here, we report that fetal testosterone measured from amniotic fluid relates positively to male-typical scores on a standardized questionnaire measure of sex-typical play in both boys and girls. These results show, for the first time, a link between fetal testosterone and the development of sex-typical play in children from the general population, and are the first data linking high levels of prenatal testosterone to increased male-typical play behavior in boys.     

DNA

The authors predict that in a few years, many areas of psychology will be awash in specific genes responsible for the widespread influence of genetics on behavior. As the focus shifts from finding genes (genomics) to understanding how genes affect behavior (behavioral genomics), it is important for the future of psychology as a science that pathways between genes and behavior be examined not only at the molecular biological level of cells or the neuroscience level of the brain but also at the psychological level of analysis. After a brief overview of quantitative genetic research, the authors describe how genes that influence complex traits like behavioral dimensions and disorders in human and nonhuman animals are being found. Finally, the authors discuss behavioral genomics and predict that DNA will revolutionize psychological research and treatment early in the 21st century.     

Audiovisual integration facilitates monkeys’ short-term memory

Many human behaviors are known to benefit from audiovisual integration, including language and communication, recognizing individuals, social decision making, and memory. Exceptionally little is known about the contributions of audiovisual integration to behavior in other primates. The current experiment investigated whether short-term memory in nonhuman primates is facilitated by the audiovisual presentation format. Three macaque monkeys that had previously learned an auditory delayed matching-to-sample (DMS) task were trained to perform a similar visual task, after which they were tested with a concurrent audiovisual DMS task with equal proportions of auditory, visual, and audiovisual trials. Parallel to outcomes in human studies, accuracy was higher and response times were faster on audiovisual trials than either unisensory trial type. Unexpectedly, two subjects exhibited superior unimodal performance on auditory trials, a finding that contrasts with previous studies, but likely reflects their training history. Our results provide the first demonstration of a bimodal memory advantage in nonhuman primates, lending further validation to their use as a model for understanding audiovisual integration and memory processing in humans.     

Biological Bases of Maternal Attachment

In recent years, there has been growing interest in investigating the processes affecting caregiving behavior. Recent studies of human and nonhuman primates have suggested that hormones can account, at least in part, for changes in caregiving motivation during pregnancy and the postpartum period and for variability in caregiving motivation and behavior among individuals. Although hormones may not be the primary determinants of caregiving, future research cannot afford to overlook the contribution that biological processes can make to normative and pathological attachment and parenting.     

How we use rules to select actions: A review of evidence from cognitive neuroscience

Much of our behavior is guided by rules, or prescribed guides for action. In this review, I consider the current state of knowledge of how rules are learned, stored in the brain, and retrieved and used as the need arises. The focus is primarily on studies in humans, but the review is informed by relevant studies in nonhuman primates. Ventrolateral prefrontal cortex (VLPFC) has been implicated in rule learning, retrieval from long-term memory, and on-line maintenance during task preparation. Interactions between VLPFC and temporal cortex are required for rule retrieval in nonhuman primates, and brain imaging findings in humans suggest that rule knowledge is stored in the posterior middle temporal gyrus. Dorsolateral PFC appears to be more closely related to rule-based response selection than to rule retrieval. An important task for the future is to explain how PFC, basal ganglia, and temporal, parietal, and motor cortices interact to produce rule-guided behavior.     

Multiple measures of motor lateralization in human primates (Homo sapiens)

Laterality was assessed in 100 human (Homo sapiens) subjects through the use of five measures of motoric behavior in three categories: locomotor, manual, postural. Locomotor measures included leading limb for initiation of walking and whole-body turning. Performance and questionnaire measures were used to assess lateral hand bias. Postural bias was assessed as the weight distribution in quiet standing. Population-level biases on the manual and leading limb measures were to the right; on posture and turning, to the left. Locomotor measures were found to be altered by marching experience. Only the manual measures were correlated. We compare the results with those of nonhuman primate studies that have used similar measures and discuss some patterns of laterality common to human and nonhuman primates.     

Dissecting adrenal and behavioral responses to stress by targeted gene inactivation in mice

To define the molecular pathways modulating adrenal and behavioral responses to stress, we have generated mice with inactivation of hypothalamic neuropeptides and signaling pathways. Studies in mice deficient in corticotropin-releasing hormone (CRH) have revealed the essential role for CRH in adrenal glucocorticoid production in response to many physiological and psychological stressors. Immune system activation in CRH-deficient mice provides a unique exception to the necessity for CRH in stimulating adrenal glucocorticoid production. By analyzing mice deficient in interleukin-6 (IL-6) and CRH, we find that restoration of glucocorticoid output with inflammation is largely mediated by dysregulated IL-6 production. Current studies focus on identifying cellular and gene targets by which glucocorticoids regulate immune system function. In contrast to impaired adrenocortical responses to stress, CRH-deficient mice exhibit normal behavioral responses to stress. To determine signaling pathways that may contribute to the behavioral responses to stress, we have generated and analyzed mice deficient in adenylyl cyclase type 8 (AC8). AC8 deficient mice have intact adrenocortical responses to stress, but an inability to undergo stress-induced alterations in behavior.     

The Development of Expertise: Animal Models?

There is a continuing debate in the psychological literature between researchers who lean more toward learning theories of expertise development and those who lean more toward talent theories. However, the development of human expertise has not been open to direct experimental methods and will probably continue to elude experimentalists in the future. A promising alternative to direct experimental methods is to use nonhuman animal models, a possibility that researchers in expertise seem to have overlooked. However, there are studies in the animal behavior literature that address the development of nonhuman animal expertise without specifically referring to the topic as expertise. In the present study, the author discusses two nonhuman animal examples of expertise development that have been researched by ethologists. Nonhuman animal expertise development, unlike human expertise development, is subject to direct experimentation. The author thus recommends that researchers use nonhuman animals in their studies of expertise.