Brian Cusato

Learning with arbitrary versus ecological conditioned stimuli: Evidence from sexual conditioning

Laboratory investigations of Pavlovian conditioning typically involve the association of an arbitrary conditioned stimulus (CS) with an unconditioned stimulus (US) that has no inherent relation to the CS. However, arbitrary CSs are unlikely to become conditioned outside the laboratory, because they do not occur often enough with the US to result in an association. Learning under natural circumstances is likely only if the CS has a preexisting relation to the US. Recent studies of sexual conditioning have shown that in contrast to an arbitrary CS, an ecologically relevant CS is resistant to blocking, extinction, and increases in the CS-US interval and results in sensitized responding and stronger secondorder conditioning. Although the mechanisms of these effects are not fully understood, these findings have shown that signature learning phenomena are significantly altered when the kinds of stimuli that are likely to become conditioned under natural circumstances are used. The implications of these findings for an ecological approach to the study of learning are discussed. An earlier version of this article was presented by M. Domjan as an invited address at the 2001 meetings of the Pavlovian Society of North America in New Brunswick, NJ. The preparation of the manuscript and the original research by the authors were supported by Grant MH 39940 from the National Institutes of Health.

Pavlovian feed-forward mechanisms in the control of social behavior

The conceptual and investigative tools for the analysis of social behavior can be expanded by integrating biological theory, control systems theory, and Pavlovian conditioning. Biological theory has focused on the costs and benefits of social behavior from ecological and evolutionary perspectives. In contrast, control systems theory is concerned with how machines achieve a particular goal or purpose. The accurate operation of a system often requires feed-forward mechanisms that adjust system performance in anticipation of future inputs. Pavlovian conditioning is ideally suited to subserve this function in behavioral systems. Pavlovian mechanisms have been demonstrated in various aspects of sexual behavior, maternal lactation, and infant suckling. Pavlovian conditioning of agonistic behavior has been also reported, and Pavlovian processes may likewise be involved in social play and social grooming. Several further lines of evidence indicate that Pavlovian conditioning can increase the efficiency and effectiveness of social interactions, thereby improving their cost/benefit ratio. We extend Pavlovian concepts beyond the traditional domain of discrete secretory and other physiological reflexes to complex real-world behavioral interactions and apply abstract laboratory analyses of the mechanisms of associative learning to the daily challenges animals face as they interact with one another in their natural environments.

Extinction of Conditioned Sexual Responses in Male Japanese Quail (Coturnix japonica): Role of Species-Typical Cues

The authors examined how a conditioned stimulus (CS) that included species-typical cues affected the acquisition and extinction of conditioned sexual responses in male quail (Coturnix japonica). Some subjects were conditioned with a CS that supported sexual responses and included a taxidermic head of a female quail. Others were conditioned with a similar CS that lacked species-typical cues. Pairing the CSs with access to live females increased CS-directed behavior, with the head CS eliciting significantly more responding than the no-head CS. Responding to the head CS persisted during the 42-day, 126-trial extinction phase; responses to the no-head CS extinguished. Responding declined when the cues were removed or the subjects were sexually satiated. Possible functions and mechanisms of these effects are discussed.

Dissociation of conditioned appetitive and consummatory sexual behavior: Satiation and extinction tests

Sexual responses were conditioned in male Japanese quail using the opportunity to copulate with a female as the unconditioned stimulus (US). The conditioned stimulus (CS) was a 3-D object made of a taxidermically prepared female quail head mounted on a terry-cloth body. Both appetitive conditioned responses (approach and proximity to the CS) and consummatory conditioned responses (mount and cloacal contact directed toward the CS) developed when 2-min presentations of the CS were followed immediately by the US, but not when the CS and US were separated by trace intervals of 10 or 20 min (Experiment 1). Postconditioning sexual satiation suppressed conditioned cloacal contact responses more than conditioned approach to the CS (Experiment 2), and “acute” extinction suppressed both conditioned mounting and conditioned cloacal contact responses more than conditioned approach to the CS (Experiment 3). These results demonstrate a functional dissociation between conditioned appetitive and consummatory responses and imply that the motivational and/or associative mechanisms underlying the two types of behavior are distinct.

Facilitation of appetitive conditioning with naturalistic conditioned stimuli: CS and US factors

Adding limited female cues to a conditioned stimulus (CS) facilitates conditioned male sexual responding. In two experiments, we examined the mechanisms of this facilitation effect. The color of the female cues on the CS was varied in Experiment 1. Similarity between the CS plumage color and the color of the live female (the unconditioned stimulus [US]) could only partially account for the results. The extent to which the facilitation effect represents a specialization of sexual behavior was examined in Experiment 2 by comparing conditioning with either food or copulation as the US. The CSs with female cues elicited more approach and grab responses regardless of which US was used. However, uniquely sexual conditioned responses (mounts and cloacal contacts) were enhanced only when sexual reinforcement served as the US. These findings suggest that the facilitation effect of female cues represents a general feature of appetitive behavior systems.

Barbados green monkeys (Chlorocebus sabaeus) recognize ancestral alarm calls after 350 years of isolation.

Vervet monkeys (Chlorocebus pygerythrus) produce alarm calls and anti-predator behaviors that are specific to a threatening predators mode of attack. Upon hearing a leopard alarm, the monkeys will run up trees where they are relatively safe. In contrast, eagle alarms prompt the monkeys to run under bushes and snake alarms stimulate bipedal standing. Early researchers proposed that the meaning of each alarm call is conveyed by observational learning. If this true then absence of the predator that elicits the alarm call may lead to alteration or decay of the alarms meaning since there is no longer opportunity for observational learning to occur. The present study tested this hypothesis by presenting alarm calls to a closely related species of monkeys (Chlorocebus sabaeus) that have been isolated from their ancestral predators for more than 350 years. The monkeys ran up trees in response to a leopard alarm, but not when the same alarm was played backwards and not in response to a snake alarm. Snake alarms failed to reliably elicit bipedal standing. These results suggest that the leopard alarm call conveys the same information to Barbados green monkeys as West African green monkeys despite generations of isolation from leopards.

A new model for sexual conditioning: the ring dove (Streptopelia risoria).

Sexual conditioning investigations have primarily used rats and domestic quail as subjects. Although much has been learned from such experiments, the relative simplicity of rat and quail reproductive behavior prohibits investigation of certain experimental questions about sexual conditioning. In contrast, the reproductive behavior of male and female ring doves (Streptopelia risoria) is complex, involving courtship, bonding, and parental care. In the present experiment, male ring doves that were presented with a visual conditioned stimulus paired with access to their pair-bonded mate (the unconditioned stimulus) showed sexual conditioned responding in the presence of the conditioned stimulus. These results represent the first evidence of sexual conditioning in ring doves and illustrate the potential of ring doves as a useful model for future sexual conditioning investigations.

Physiological responses and political behavior: Three reproductions using a novel dataset

One of the most provocative recent findings in our understanding of political behavior is the link between physiological responses to environmental stimuli and political attitudes and behavior. This line of research holds much promise in explaining some of the foundational evolutionary origins of basic political orientations. Much of this recent research focused specifically on skin conductance response to threatening and disgusting stimuli, however, is based on analyses of a data collection sample of approximately 200 study participants drawn from the same community at a single point in time. Herein we attempt to reproduce many of the basic findings of recent research on skin conductance response and political behavior using data collected from a novel and unique dataset in a different context. In brief, we fail to reproduce many of the basic findings from this incipient line of research which suggests that the link between skin conductance and political behavior may be more contingent than previously assumed.

Mate reinforcement value and the pair bond in ring neck dove (Streptopelia risoria)

During the breeding season, monogamous birds form partnerships characterized by preferential involvement in reproductive and parental behaviors with a mate. The breeding partnership is dependent on a ‘pair bond’, an adhesive force that promotes prolonged affiliation and behavioral cooperation between two birds. Here we propose that the adhesive force of the pair bond is at least partially the result of the acquired reinforcement value of the mate. If the mate becomes a reinforcer during courtship then through classical conditioning principles the mate will reinforce affiliative behavior evident in pair-bonded birds. The present experiments were designed to determine whether the pair-bonded mate of ring neck dove (Streptopelia risoria) acquire reinforcement value during the reproductive cycle. Mate reinforcement value was assessed using a conditioned place preference paradigm in which the mate was paired with a visually distinct context and a second distinct context was paired with social isolation (Experiment 1) or an unfamiliar bird of the opposite sex (Experiment 2). Both males and females preferred the context that had been paired with the mate to the context paired with social isolation or an unfamiliar dove. The results suggest that pair-bonded mates are stronger reinforcers than unfamiliar birds. Experiment 3 found that the preference for the mate context over the unfamiliar dove context was stronger during incubation than during courtship. The possible involvement of a classical conditioning process in the maintenance of the pair bond is discussed.

Threats from the past: Barbados green monkeys (Chlorocebus sabaeus) fear leopards after centuries of isolation

Ability to recognize and differentiate between predators and non-predators is a crucial component of successful anti-predator behavior. While there is evidence that both genetic and experiential mechanisms mediate anti-predator behaviors in various animal species, it is unknown to what extent each of these two mechanisms are utilized by the green monkey (Chlorocebus sabaeus). Green monkeys on the West Indies island of Barbados offer a unique opportunity to investigate the underpinnings of anti-predator behaviors in a species that has been isolated from ancestral predators for over 350 years. In the first experiment, monkeys in two free-ranging troops were presented with photographs of an ancestral predator (leopard, Panthera pardus) and a non-predator (African Buffalo, Syncerus caffer). Relative to non-predator stimuli, images of a leopard elicited less approach, more alarm calls, and more escape responses. Subsequent experiments were conducted to determine whether the monkeys were responding to a leopard-specific feature (spotted fur) or a general predator feature (forward facing eyes). The monkeys showed similar approach to images of an unfamiliar non-predator regardless of whether the image had forward facing predator eyes or side facing non-predator eyes. However, once near the images, the monkeys were less likely to reach for peanuts near the predator eyes than the non-predator eyes. The monkeys avoided an image of spotted leopard fur but approached the same image of fur when the dark spots had been removed. Taken together, the results suggest that green monkey anti-predator behavior is at least partially mediated by genetic factors.