Contextual conditioning and the control of copulatory behavior by species-specific sign stimuli in male Japanese quail

Three experiments were conducted to identify species-specific sign stimuli sufficient to elicit copulatory behavior in male Japanese quail and to determine how learning is involved in the control of behavior by these sign stimuli. In Experiment 1, sexually experienced subjects were tested for copulatory behavior with a live female quail and with a model consisting of a female quail's head and neck mounted in front of a foam pad. Comparable levels of copulatory behavior were observed in the two tests, indicating that static visual cues provided by a female quail's head and neck are sufficient to elicit copulatory behavior in this species. Experiment 2 showed that male birds that previously received numerous opportunities to copulate with a live female quail in the test situation were significantly more likely to copulate with the head + neck model than were sexually inexperienced subjects. Experiment 3 showed that prior sexual experience with live quail facilitated responding to the head + neck model only if the sexual experience was provided in the same place where subjects were later tested with the model. This last finding suggests that sexual experience facilitates control of copulatory behavior by species-specific sign stimuli through contextual conditioning. Contextual conditioning may lower the threshold for sexual behavior with the result that a stimulus as impoverished as an immobile model containing only the head and neck of a female quail becomes sufficient to elicit normal levels of copulatory behavior. The results are also discussed as an example of conditioned stimulus facilitation of responding to an unconditioned stimulus.     

Formulation of a behavior system for sexual conditioning

Empirical and conceptual developments that led to the formulation of a behavior system for the sexual conditioning of male Japanese quail are described. Initial efforts concentrated on conditioning with localized conditioned stimuli and on identifying behavioral indices of conditioning. Later, learning about species-typical cues and about contextual cues was also explored, and it became evident that different types of cues control different aspects of sexual behavior. The results were used to formulate a behavior system containing both response and stimulus dimensions. In this system, contextual cues and local cues are assumed to elicit only general search behavior unconditionally. In contrast, unconditioned responses to species-typical cues of a female quail include general search, focal search, and copulatory behavior. General search, focal search, and copulatory behavior can become conditioned to local cues. Conditioning can also modify focal search behavior elicited by species-typical cues and can result in various modulatory influences between different types of stimuli. The behavior system approach provides a framework for organizing the diverse sexual conditioning effects and suggests future directions for investigation.     

An animal model of fetishism

An animal model of sexual fetishism was developed with male Japanese quail based on persistence of conditioned sexual responding during extinction to an inanimate object made of terrycloth (Experiments 1 and 3). This persistent responding occurred only in subjects that came to copulate with the terrycloth object, suggesting that the copulatory behavior served to maintain the fetishistic behavior. Sexual conditioning was carried out by pairing a conditioned stimulus (CS) with the opportunity to copulate with a female (the unconditioned stimulus or US). Copulation with the CS object and persistent responding did not develop if the CS was a light (Experiment 1) or if conditioning was carried out with a food US (Experiment 2). In addition, subjects that showed persistence in responding to the terrycloth CS did not persist in their responding to a light CS (Experiment 3). The results are consistent with the hypothesis that conditioned copulatory behavior creates a form of self-maintenance that leads to persistent responding to an inanimate object. The development of an animal model of such fetishistic behavior should facilitate experimental analysis of the phenomenon.     

Increased responding to female stimuli as a result of sexual experience: Tests of mechanisms of learning

Sexual experience increases the response of males to stimuli provided by female conspecifics in a variety of species. The mechanisms of learning involved in this type of phenomenon were explored in two experiments with Japanese quail. The results indicated that instrumental conditioning with copulatory opportunity is not necessary for the acquisition of responding to female cues, and responding is not facilitated by learning about the location of the female. However, the response of males to female stimuli (as well as to arbitrary stimuli associated with access to a female) was enhanced by the presence of sexually conditioned contextual cues. Substantial levels of responding also occurred to female stimuli in a context where the subjects never encountered a female quail before. This latter outcome is consistent with the possibility that stimuli from a female become directly associated with sexual reinforcement during the course of sexual experience. Similar forms of learning may be involved in the effects of sexual experience on the response of mammalian species to female odours.     

The Adaptive Significance of Sexual Conditioning: Pavlovian Control of Sperm Release

Male quail received Pavlovian conditioning trials that consisted of placement in a distinctive experimental chamber (the conditioned stimulus) paired with the opportunity to copulate with a female (the unconditioned stimulus). For control subjects, exposures to the conditioned and unconditioned stimuli were unpaired. After four and six trials, each subject was placed in the experimental chamber with a probe stimulus that included some of the visual cues of a female's head and neck. Pavlovian conditioning increased how much time subjects spent near the probe stimulus. Conditioned subjects also released greater volumes of semen and greater numbers of spermatozoa than the control subjects. Significant differences were not obtained in serum testosterone levels or in other measures of sperm quality. These results demonstrate that sexual Pavlovian conditioning can affect reflexes involved in sperm release and thereby modulate reproductive fitness.     

One-trial appetitive conditioning in the sexual behavior system

One-trial Pavlovian conditioning has been demonstrated with aversive reinforcers such as electric shock and lithium chloride. The present experiments using male Japanese quail were conducted to determine if an appetitive unconditioned stimulus (US), the opportunity to copulate with a female quail, can also generate one-trial learning. In Experiment 1, subjects were exposed to a contextual conditioned stimulus (CS) for 35 sec and then given copulatory opportunity. In Experiment 2, male birds were given 0, 2, or 4 min of exposure to the contextual CS before presentation of a female. In both cases, control groups received comparable exposure to both the contextual CS and the sexual US, but in an unpaired fashion. Subjects were tested for sexual learning by reintroducing them to the experimental context in the presence of a test object that incorporated the taxidermically prepared head of a female quail. In both Experiments 1 and 2, subjects for whom the contextual CS and sexual US had been paired displayed significantly more approach to the test object than did unpaired subjects.     

Sexual fetishism in a quail (Coturnix japonica) model system: test of reproductive success

In the present study, the authors explored the reproductive consequences of fetishistic behavior in a previously developed animal model of sexual fetishism (F. K?ksal et al., 2004). Male domesticated quail (Coturnix japonica) received sexual conditioning trials in which a terrycloth object (the conditioned stimulus [CS]) was paired with the opportunity to copulate with a female quail (the unconditioned stimulus). Approximately half of the male quail came to copulate with the CS object and were considered to have developed fetishistic behavior. Each of the male quail was then tested with a female quail, whose eggs were incubated to determine rates of fertilization. The CS object was present for 30 s before and during the copulation test. Fetishistic male quail were slower to achieve cloacal contact with the female quail and showed less efficient copulatory behavior. However, they fertilized a greater proportion of eggs than nonfetishistic male quail. These results are unexpected from previous studies of the relationship between reproductive success and copulatory behavior and are discussed in terms of how fetishistic behavior directed toward an inanimate object may modify male-female interactions.     

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.     

CLASSICAL CONDITIONING OF COURTING BEHAVIOR IN THE JAPANESE QUAIL,COTURNIX COTURNIX JAPONICA1

Male Japanese quail were classically conditioned to display courting behavior at the sound of a buzzer, a previously neutral stimulus. The buzzer (conditioned stimulus) was paired with the presentation of a female quail (unconditioned stimulus) for a number of trials. The courting display, invariably elicited from the male by the presentation of the female, began to appear in part to the conditioned stimulus as early as the fifth pairing. All components of the display were elicited from all birds by the conditioned stimulus alone within 32 pairings of the conditioned and unconditioned stimuli.     

Topography of spatially directed conditioned responding: effects of context and trial duration

Domesticated quail (Coturnix japonica) received a discrete conditioned stimulus (CS) at one end of the experimental chamber paired with the opportunity to copulate with a female quail (the unconditioned stimulus) in a goal box located 112 cm away. Approach to the CS (sign tracking) and approach to the goal area (goal tracking) were measured. The duration of exposure to the experimental context (C) was varied in Experiment 1, and the duration of the conditioning trials (T) was varied in Experiment 2 for independent groups, creating C/T ratios of 1.0, 1.5, 4.5, 45, and 180. Contrary to previous reports of a direct relation between the C/T ratio and conditioned responding, in the present experiments, a shift in the topography and stimulus control of conditioned behavior occurred. Low C/T ratios (1.0-4.5) produced goal tracking controlled by contextual cues, whereas high C/T ratios (45 and 180) produced sign tracking controlled by the discrete CS.     

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.     

Sexual Pavlovian conditioned approach behavior in male Japanese quail (Coturnix coturnix japonica)

A localized visual stimulus presented immediately prior to access to a female conspecific stimulated approach behavior in male Japanese quail after several conditioning trials. Development of this conditioned approach behavior was observed with two different types of signal lights, 10-s and 30-s signal durations, large and small experimental chambers, and with male birds housed continually in the conditioning chambers or only placed in the chamber for brief daily sessions. Conditioning also resulted in shorter latencies to initiate copulation in males given access to a female following the signal light, in comparison with males that received access to a female unannounced by the light. Although some aspects of the conditioning experience were retained over a 6-week interval, some loss of the behavior was also observed. The conditioned behavior also decreased with repeated extinction trials, during which the signal light was presented in the absence of access to a female conspecific. The results are discussed in relation to other aspects of the social behavior of Japanese quail and other studies of sexual conditioning.     

One-month-old human infants learn about the social world while they sleep

Although infants display preferences for social stimuli early in their lives, we know relatively little about the mechanisms of infant learning about the social world. In the current set of studies, 1-month-old infants underwent an adapted eyeblink conditioning paradigm to examine learning to both 'social' and non-social cues. While infants were asleep, they were presented with either a 'social' stimulus (a female voice) or one of two non-social stimuli (tone or backward voice) followed by an airpuff presented to the eyelid. Infants in the experimental groups displayed increased learning across trials, regardless of stimulus type. However, infants conditioned to the 'social' stimulus showed increased learning compared to infants conditioned to either of the non-social stimuli. These results suggest a mechanism by which learning about the social world occurs early in life and the power of ecologically valid cues in facilitating that learning.     

Pavlovian conditioning in human skilled motor behavior

The role of Pavlovian contingencies in human skilled motor behavior was investigated in three experiments by means of a new conditioning preparation. In Experiment 1 the present method was shown to be appropriate for the study of associative learning. Subjects who experienced a standard delay configuration performed significantly more conditioned responses than subjects who received either backward conditioning or random pairings. Stimulus generalization was shown to be slight in two additional groups. Subsequent experiments examined conditioning with multiple conditioned stimuli (CSs). In particular, in Experiment 2 some reciprocal overshadowing was demonstrated when two conditional stimuli (tone and vibration) were compounded. Experiment 3 investigated blocking. Blocking was less than expected, however. Subjects’ perceptions of the stimuli and reaction time data suggest that a certain proportion had shifted their attention to the added element of the CS compound. Results are discussed in relation to other studies on Pavlovian learning in humans and animals, which are concerned with “stimulus selection.”     

The role of cuticular pheromones in courtship conditioning of Drosophila males

Courtship conditioning is an associative learning paradigm in Drosophila melanogaster, wherein male courtship behavior is modified by experience with unreceptive, previously mated females. While the training experience with mated females involves multiple sensory and behavioral interactions, we hypothesized that female cuticular hydrocarbons function as a specific chemosensory conditioned stimulus in this learning paradigm. The effects of training with mated females were determined in courtship tests with either wild-type virgin females as courtship targets, or with target flies of different genotypes that express distinct cuticular hydrocarbon (CH) profiles. Results of tests with female targets that lacked the normal CH profile, and with male targets that expressed typically female CH profiles, indicated that components of this CH profile are both necessary and sufficient cues to elicit the effects of conditioning. Results with additional targets indicated that the female-specific 7,11-dienes, which induce naive males to court, are not essential components of the conditioned stimulus. Rather, the learned response was significantly correlated with the levels of 9-pentacosene (9-P), a compound found in both males and females of many Drosophila strains and species. Adding 9-P to target flies showed that it stimulates courting males to attempt to copulate, and confirmed its role as a component of the conditioned stimulus by demonstrating dose-dependent increases in the expression of the learned response. Thus, 9-P can contribute significantly to the conditioned suppression of male courtship toward targets that express this pheromone.     

One-trial learning and superior resistance to extinction of autonomic responses conditioned to potentially phobic stimuli.

Human subjects were exposed to pictures of potentially phobic (snakes) and supposedly neutral (houses) objects as conditioned stimuli (CSs) in a Pavlovian conditioning experiment with shock as unconditioned stimulus (US), and skin conductance and finger pulse volume as dependent variables. The skin conductance responses conditioned to phobic stimuli were acquired after one CS-US pairing, and showed practically no extinction, whereas the responses to neutral stimuli showed very little resistance to extinction after both 1 and 5 reinforcements. The superior resistance to extinction of the phobic condition was interpreted to be a specific associative effect. In general, the skin conductance acquisition data showed tendencies similar to those during extinction. For finger pulse volume responses, however, there were very weak conditioning effects, and no effect of stimulus.     

Stimulus generalization as a function of stimulus novelty and familiarity in rats

Three experiments used rats as subjects to investigate the generalization of conditioned responding between stimuli as a function of the subjects' exposure to these cues prior to conditioning. Experiment 1 used a between-subjects design, food as the reinforcer, and measured the tendency of subjects to approach the site of food delivery during the stimuli. Generalization of this response was more marked when the training and test stimuli were equated in terms of their novelty (i.e., when both were novel or both were familiar) than when the stimuli differed in this respect (i.e., when one was novel and the other was familiar). Experiments 2a and 2b used within-subjects designs to confirm the reliability of the results of Experiment 1. Implications of these results for current theories of stimulus representation are discussed.     

Differential effects of omission contingencies on various components of Pavlovian appetitive conditioned responding in rats

Five experiments with rat subjects investigated the effects of omission and partial reinforcement contingencies on five individual behaviors evoked by visual and auditory conditioned stimuli paired with a food unconditioned stimulus. The effects of omission depended on the behavior on which that contingency was placed: One behavior was eliminated, one was unaffected, and three were reduced relative to the performance of yoked controls. Partial reinforcement resulted in lower frequencies of three behaviors and higher frequencies of two behaviors, compared with performance under consistent reinforcement. A partial reinforcement extinction effect was noted with one behavior but not with the others. These results are related to the possible role of instrumental conditioning contingencies in generating conditioned behavior in this appetitive conditioning preparation and to the independence of individual components of a complex conditioned response.     

Separating discriminative and function-altering effects of verbal stimuli

Ever since Skinner's first discussion of rule-governed behavior, behavior analysts have continued to define rules, either explicitly or implicitly, as verbal discriminative stimuli. Consequently, it is not difficult to find, in the literature on rule-governed behavior, references to stimulus control, antecedent control, or to rules occasioning behavior. However, some verbal stimuli have effects on behavior that are not easily described as discriminative. Such stimuli don't evoke behavior as discriminative stimuli, but rather alter the functions of other stimuli in a manner analogous to operant and respondent conditioning. Hence, this type of control has been called function altering. Any known stimulus function (e.g., evocative, or [conditioned] reinforcing or punishing functions) can apparently be altered by such function-altering stimuli. Describing these stimuli as discriminative stimuli obscures their possible function-altering effects and consequently may retard inquiry into them. This paper encourages behavior analysts to begin separating the discriminative and function-altering effects of verbal stimuli and suggests that by doing so, behavior analysts may better understand what may be most unique about these stimuli. Results from several experiments, especially those in which children served as subjects, are analyzed. Finally, some speculations are offered concerning the genesis of function-altering stimuli.     

The nature of sexual reinforcement.

Sexual reinforcers are not part of a regulatory system involved in the maintenance of critical metabolic processes, they differ for males and females, they differ as a function of species and mating system, and they show ontogenetic and seasonal changes related to endocrine conditions. Exposure to a member of the opposite sex without copulation can be sufficient for sexual reinforcement. However, copulatory access is a stronger reinforcer, and copulatory opportunity can serve to enhance the reinforcing efficacy of stimulus features of a sexual partner. Conversely, under certain conditions, noncopulatory exposure serves to decrease reinforcer efficacy. Many common learning phenomena such as acquisition, extinction, discrimination learning, second-order conditioning, and latent inhibition have been demonstrated in sexual conditioning. These observations extend the generality of findings obtained with more conventional reinforcers, but the mechanisms of these effects and their gender and species specificity remain to be explored.