Learning associations involving predators and non-predators in infancy

Fear is one of the most universal human emotions and many common fears, such as aversions toward predatory animals, has been observed cross-culturally. Previous research has indicated that humans have an evolved predator detection mechanism (Mineka & Ohman, 2002). The present research explored this innate predator detection mechanism in infants by testing whether they are able to learn associations involving predators more quickly than associations involving non-predators. Eleven-month-old infants were shown images of snakes, spiders, flowers, and mushrooms paired with happy or scared faces. Infants’ looking times were recorded to determine differences in how quickly they learned associations involving predators and non-predators. In addition, looking times were recorded to determine differences in the increase of attention to novel stimuli following habituation to predators and to non-predators. The results indicate that there was no difference in looking times between predator and nonpredator stimuli during the habituation phase and did not show a differential increase in attention to predator stimuli and non-predator stimuli following habituation. Future research is needed to further investigate this mechanism in infants. Learning Associations 3 All species face adaptive problems that need to be solved in order for an organism to survive and reproduce. Some of these adaptive problems include finding food, securing a mate, and avoiding predators. The adaptations that have emerged to overcome these problems are designed by natural selection and are often specific to the environment in which they evolved. Although animal studies detailing such evolutionary adaptations are prevalent, little is known regarding similar mechanisms in humans. Humans today exist in an environment very different from the one in which they initially evolved, making evolutionary adaptations difficult to recognize. It is still apparent, however, that humans have evolved psychological mechanisms as a result of the adaptive problems faced by our early ancestors. One such mechanism is the ability to detect and respond to predators. Even though the threat of predators does not greatly effect the survival of modern humans, avoiding animals such as snakes and spiders, was critical to the survival of our ancestors. Those who failed successfully to avoid these predators risked injury or death, and would be much less likely to survive long enough to reproduce. Research on Animals All types of animals face the threat of predators on a regular basis. In order for these animals to survive, evolution has shaped mechanisms in animals that allows them to detect and responds to predators in ways that increase their chance of survival. A significant amount of evidence reveals innate predator detection and response behaviors in the animal kingdom. The velvet gecko has the ability to detect chemical cues from the broadheaded snake, its primary predator, and discriminate between these cues and those of non-predatory snakes living in the same environment (Downes & Shine, 1998). Learning Associations 4 Having detected these chemical cues, the velvet gecko proceeds to respond in unique ways, pressing itself flat against the ground in order to avoid detection, and if detected, raising its tail to direct the forthcoming attack away from its body and to its tail (Downes & Shine, 1998). In addition, the moustached warbler displays several distinct responses to predators. The mother warbler will give an alarm call to warn her chicks of potential danger, however, a warbler without chicks will not alarm call in response to predators. The alarm calls are specific to the type of danger present. After hearing the alarm call, the chicks will either jump in response to a terrestrial predator such as a human or snake or duck in response to an aerial predator such as a marsh harrier. These specific responses to predators are present just days after hatching, indicating that they are innate responses and not the result of learning alone (Kleindorfer, Hoi, & Fessl, 1996). The moustached warbler has evolved specific alarm calls to warn their chicks of potential danger and selective responses that are contingent on the type of predator (Kleindorfer, Hoi, & Fessl, 1996). Primates often use alarm calls as a response to predators. In particular, the Diana monkeys have evolved two particular defense strategies to protect themselves from their two main predators, the leopard and the chimpanzee (Zuberbuhler, 2000). Diana monkeys will create several loud, conspicuous alarm calls in response to a leopard. This signal warns other monkeys of the potential threat and informs the leopard that they have been detected. At this point, the leopard usually retreats. In contrast, Diana monkeys will remain silent and flee the scene if a chimpanzee is present. Since chimpanzees are good climbers, giving an alarm call would make the Diana monkey’s location available to the chimpanzee and would most likely result in capture. The Diana monkey, therefore, Learning Associations 5 remains silent and attempts to flee in order to avoid the predator. The two distinct responses to two different predators indicate that evolution has helped shape the Diana monkeys’ responses to specific potential threats (Zuberbuhler, 2000). Other types of primates also show specific responses to predators. Research by Mineka, Davidson, Cook, and Keir (1984) on rhesus monkeys indicates that a fear response to predators might not actually be present at birth; rather rhesus monkeys have a predisposition to learn fear responses to predators. When lab reared monkeys that initially did not show a fear response to snakes observed a model monkey behaving fearfully in the presence of a snake, the lab reared monkey quickly developed an intense and long-lasting fear of snakes. The lab reared monkeys did not develop this fear response for neutral stimuli, such as flowers or toy rabbits (Mineka et al., 1984). This indicates that rhesus monkeys are predisposed to learn fear responses to snakes, a natural predator, but not non-threatening stimuli, and will learn these strong fear responses quickly and with very little exposure to the modeled fear response. Research on Humans Similar to other animals, there is evidence that humans have evolved a psychological mechanism specific for predator detection and response. These mechanisms evolved in ancestral humans during a time when predators were a constant threat to survival. Even though most modern humans currently live in an environment in which they rarely face predators, the evolved predator detection and response mechanism is still apparent. This mechanism would allow ancestral humans to detect and avoid sources of danger with very fast activation of defensive behaviors (Mineka & Ohman, 2002). This evolved predator detection and response mechanism must have several Learning Associations 6 specific characteristics in order for it to be beneficial. The mechanism must be highly selective with regard to input, principally responding to threatening stimuli in its evolutionary environment. It must be automatic in that it takes only a small amount of neural computations to identify stimuli and immediately give them priority. This mechanism must be encapsulated within itself, causing processes associated with this module to be carried out without interruption. Finally, this mechanism must be associated with specific neural circuitry shaped by evolution. In humans, and in other mammals, it is located in part of the subcortical area of the brain, known as the amygdala, and controls various fear behaviors (Ohman & Mineka, 2001). Research on physiological responses to fear, common phobias, speed of detection of predator stimuli versus non-predator stimuli, automatic responses to predator stimuli, and infants looking responses to predator stimuli has provided evidence that this mechanism exists in humans and functions according to these principles. This psychological mechanism includes an evolved adaptation to respond to potentially threatening predators in a way that increases the chance of survival. Showing a fear response to potentially threatening stimuli is a beneficial response to predators, causing the organism to respond in an appropriate way in order to increase their chance of survival. Physiological responses associated with fear in humans include an increase in heart rate, blood pressure, and eye movement (Sinha & Parsons, 1996). These physiological responses prepare the individual to behave in certain ways, such as fighting or fleeing the situation, in order deal with the potential threat (Ohman & Mineka, 2003). Research on phobias reveals that humans are far more likely to develop fears of objects that were potentially dangerous or harmful to early humans, and for which the Learning Associations 7 ability to recognize and respond quickly to these potential dangers would have been advantageous for one’s survival and reproduction (Hofman, Moscovitch, & Heinrichs, 2002). It is those natural threats, such as predators or heights, which are strongly associated with fear in modern humans (Van den Berg & Heijne, 2005). In contrast, humans are far less likely to develop fears to dangers in the modern environment (Buss, 2004). This explains why fear of spiders and snakes are significantly more common than fear of guns or automobiles, even though the latter is currently much more dangerous to humans than the former. Predator detection is a critical aspect of the psychological mechanism that evolved in order to protect early humans from predators. This predator detection mechanism is selectively sensitive to and automatically activated by predator stimuli, such as snakes and spiders (Ohman & Mineka, 2003). Ohman, Flykt, and Esteves (2001) investigated this module by examining whether adult participants would detect images of fear-relevant stimuli, such as snakes and spiders, against a background of fear-irrelevant stimuli, such as mushrooms and flowers, faster than fear-irrelevant stimuli hidden against a background of fear-relevant stimuli. Participants were significantly faster in detecting fear-relevant target items among fear-irrelevant distracters than vise versa (Ohman et al., 2001). Ohman et al. (2001) concluded that people automatically attended to stimuli involving some degree of threat, but do not for non-threatening stimuli. Research by Globisch, Hamm, Esteves, and Ohman (1999) further showed the automatic nature of the predator detection and response mechanism. Subjects with high levels of fear of snakes or spiders were shown pictures of the fear-eliciting animal and pictures of neutral stimuli (such as mushrooms and flowers). Participants reliably Learning Associations 8 showed a startle eye blink response while viewing the fear-eliciting pictures but not the neutral pictures. In addition, the fear-eliciting stimuli were also associated with an increase in sweat gland activity and cardiac acceleration. This shows the automatic and unconscious processing of the fear-eliciting information. Furthermore, when the picture was shown for a very brief period of time, the startle eye blink response still occurred, even after the fear-eliciting picture was no longer present. Globisch et al. (1999) argued that the startle response still occurred in this situation because once the fear module is activated, automatic processing of the information occurs, producing a fear response that cannot be terminated, even when the fear-eliciting stimuli is removed. Research by Gerull and Rapee (2002) demonstrated how humans may be prepared to learn fear of certain stimuli by showing that toddlers can learn emotional associations to novel, fear-relevant stimuli quickly and persistently. Toddlers ranging from 15 months to 20 months were shown two novel, fear-eliciting toys: a snake and a spider. The child’s mother paired either positive or negative emotions with each toy for a duration of one minute. In response, the children adopted the emotional reaction of their mother, showing strong avoidance and fear when their mother displayed negative emotions and approaching the toy when the mother displayed positive emotions. Even after a ten minute delay, the children still displayed the same response, indicating that the toddlers formed a persistent association between the fear-relevant stimuli and their mother’s response (Gerull & Rapee, 2002). The study by Gerull and Rapee (2002) also revealed in interesting sex difference; while both males and females showed an equal amount of approaching behavior in response to their mother’s positive response, females showed greater fear than males Learning Associations 9 following the mother’s negative response to the toy. This result is consistent with evidence on the prevalence of phobias in adults. Women are almost four times more likely to have phobias of snakes or spiders than men (Fredrikson, Annas, Fischer, & Wik, 1996). This can be explained by the behavior of ancestral humans. Ancestral women spent a significant amount of time gathering food while men spent their time hunting (Buss, 2004). Unlike hunting, gathering involved close contact with vegetation in the forests and grasslands. This presented ancestral women with substantial risks, including bites from poisonous creatures, such as snake and spiders, which live in this vegetation (Buss, 2004). It would have been more beneficial for ancestral women to fear snakes and spiders than men because they were more likely to come in contact with these threats. Ancestral women also spent a significant amount of time caring for their children. Women would bring their infants and children with them as they gathered food (Buss, 2004). Because infants and children would have also been in close contact with threats such as snakes and spiders on a regular basis, evolution shaped an innate predator detection and response mechanism designed to help protect children and infants from these threats. Research conducted by Rakison and Derringer (under review) supported a predator detection mechanism that is present in infancy. Infants were shown images of a geometric spider, a spider with reconfigured features, and a completely scrambled, linear image of a spider that moved back and forth across a screen. The results revealed that infants at 5 months of age would track the image of a schematic spider significantly longer than the images of a spider with reconfigured features or a completely scrambled, linear image of a spider. These results suggest that infants may possess an innate perceptual template for spiders, causing them to pay attention to images of spiders. In Learning Associations 10 addition, research conducted by Rakison (2005) further supports an innate predator detection mechanism. Ten month old infants were familiarized with predatory animals (e.g. snakes) and then shown a familiar predator (e.g. another snake), a novel predator (e.g. a spider), and a non-predator (e.g. a rabbit). Infants looked at the novel predator and the familiar predator for the same amount of time, but looked significantly longer at the non-predatory animals than at novel predatory animals. This further indicates that infants may have an innate template for predators, causing them group different predators (e.g. snakes and spiders) into the same category and treat them similarly. The Current Study Although the results of previous research are promising, research on an evolved predator detection and response mechanism in humans is limited. The current study was designed to expand upon previous research by investigating the innate predator detection mechanisms in infants. If infants possess an evolved predator detection mechanism, they will be more likely to learn associations involving predators than associations involving non-predators and will learn associations involving predators more quickly than associations involving non-predators. More specifically, it was predicted that infants will require fewer trials to habituate to predator stimuli than to non-predator stimuli and infants will overall spend less time looking at predator stimuli than non-predator stimuli during the habituation phase. The habituation paradigm is a commonly used assessment of infant learning; infants respond less to previously experienced stimuli and relatively more to novel stimuli (Siegler, Deloache, & Eisenberg, 2003). Thomas and Gilmore (2004) explain the habituation behavior in terms of the comparator theory. This theory explains that infants Learning Associations 11 attend to a stimulus in order to form an internal representation of that stimulus. With repeated presentations of the same stimulus, the internal representation of that stimulus becomes more accurate and resembles the external stimulus more closely. Habituation occurs when then infant reduces visual attention to the stimulus, showing that the internal representation of that stimulus matches that of the external image of the stimulus. If infants have an innate template for predators, they already possess an internal representation of predators to some extent. Infants do not possess this internal representation of non-predators, however. In the present study, infants were expected to habituate in less trials and in less time to predator stimuli because there is a smaller difference between their internal representation of predator stimuli and the actual external predator stimuli than there is for non-predator stimuli. An alternative explanation to differences in the number of trials to habituate and the total looking time during habituation between predator and non-predator stimuli relates to individual differences in the general fearfulness of infants. Rieser-Danner (2003) tested 12-month-old infants in a basic-level categorization task using the habituation paradigm. Infants’ fear level was determined by a fear scale completed by the mother. The results revealed that highly fearful infants were less likely to meet the habituation criterion than were less fearful infants. In addition, highly fearful infants required more trials to habituate than less fearful infants (Rieser-Danner, 2003). Moehler, Kagan, Parzer, Wiebel, Brunner, and Resch (2006) also showed a relationship between rate of habituation and fear. Infants were tested at two weeks of age and again at 14 months. They found that infants who had a lower speed of habituation at two weeks were more fearful at 14 months. The researchers proposed that infants who habituate Learning Associations 12 faster towards a novel stimulus shortly after birth seem to be less disturbed by novel stimuli later in life (Moehler, Kagan, Parzer, Wiebel, Brunner, & Resch, 2006). This research suggests that infants will look longer and take more trials to habituate to predator stimuli than to non-predator stimuli, a suggestion in opposition to the proposed hypothesis. Although this research shows that infants who take longer to habituate are more fearful, these studies focus on individual differences between infants’ rate of habituation to the same non-fearful stimuli. Infants that were more fearful in general took longer to habituate than non-fearful infants (Rieser-Danner, 2003; Moehler, Kagan, Parzer, Wiebel, Brunner, & Resch, 2006). In the present study, infants were shown two different types of stimuli, predator and non-predator. Although predator stimuli may be fear-eliciting, infants were expected to habituate more quickly to these stimuli because of their innate template for predators. This template allows infants to attend to predator stimuli for less time than non-predator stimuli because they already possess an internal representation of predators, but do not possess this representation for non-predators. Therefore, it was predicted that infants would take fewer trials to habituate and would take less time overall to habituate to predator stimuli than to non-predator stimuli. It was also predicted that infants would increase looking time to an association involving a non-predator and a face after habituating to a different non-predator associated with a different face to a greater extent than they would for an association involving a predator and a face after habituating to a different predator associated with a different face. This differential increase in looking time is a result of the infants’ ability to group predators into the same category but not non-predators. The increase in looking Learning Associations 13 time for associations involving predators is only a result of the different face the predator is paired with and not because of the different predator. For non-predators, however, the increase in looking time is a result of a different face and a different non-predator. Because there are two novel stimuli in the non-predator condition but only one novel stimulus in the predator condition, it is predicted that infants will look longer at the nonpredator associations than the predator associations during dishabituation.