Beyond awareness and resources: Evaluative conditioning may be sensitive to processing goals

Evaluative conditioning (EC) is often regarded as an automatic affective learning process. Yet, recent empirical evidence suggests that EC may actually be sensitive to contingency awareness and to the availability of attentional resources. Here, we examine for the first time a third horseman of EC automaticity: processing goals. Specifically, we had participants engage an EC task after completing a task known to elicit the goal of processing either the perceptual similarities or the perceptual differences between stimuli. EC was predicted and found to be larger in the former (similarity-focus) than in the latter (difference-focus) condition. This finding provides original evidence that EC is sensitive to the processing goal activated in participants as they encode the CS-US pairings. The theoretical implications of this finding are discussed.     

Learning strategies during fear conditioning

This paper describes a model of fear learning, in which subjects have an option of behavioral responses to impending social defeat. The model generates two types of learning: social avoidance and classical conditioning, dependent upon (1) escape from or (2) social subordination to an aggressor. We hypothesized that social stress provides the impetus as well as the necessary information to stimulate dichotomous goal-oriented learning. Specialized tanks were constructed to subject rainbow trout to a conditioning paradigm where the conditioned stimulus (CS) is cessation of tank water flow (water off) and the unconditioned stimulus (US) is social aggression from a larger conspecific. Following seven daily CS/US pairings, approximately half of the test fish learned to consistently escape the aggression to a neutral chamber through a small escape hole available only during the interaction. The learning curve for escaping fish was dramatic, with an 1100% improvement in escape time over 7 days. Fish that did not escape exhibited a 400% increase in plasma cortisol and altered brain monoamine response to presentation of the CS alone. Elevated plasma cortisol levels represent classical fear conditioning in non-escaping fish, while a lack of fear conditioning and a decreased latency to escape over the training period in escapers indicates learned escape.     

Perceptual specialization and configural face processing in infancy

Adults’ face processing expertise includes sensitivity to second-order configural information (spatial relations among features such as distance between eyes). Prior research indicates that infants process this information in female faces. In the current experiments, 9-month-olds discriminated spacing changes in upright human male and monkey faces but not in inverted faces. However, they failed to process matching changes in upright house stimuli. A similar pattern of performance was exhibited by 5-month-olds. Thus, 5- and 9-month-olds exhibited specialization by processing configural information in upright primate faces but not in houses or inverted faces. This finding suggests that, even early in life, infants treat faces in a special manner by responding to changes in configural information more readily in faces than in non-face stimuli. However, previously reported differences in infants’ processing of human versus monkey faces at 9 months of age (but not at younger ages), which have been associated with perceptual narrowing, were not evident in the current study. Thus, perceptual narrowing is not absolute in the sense of loss of the ability to process information from other species’ faces at older ages.     

A model of amygdala–hippocampal–prefrontal interaction in fear conditioning and extinction in animals

Empirical research has shown that the amygdala, hippocampus, and ventromedial prefrontal cortex (vmPFC) are involved in fear conditioning. However, the functional contribution of each brain area and the nature of their interactions are not clearly understood. Here, we extend existing neural network models of the functional roles of the hippocampus in classical conditioning to include interactions with the amygdala and prefrontal cortex. We apply the model to fear conditioning, in which animals learn physiological (e.g. heart rate) and behavioral (e.g. freezing) responses to stimuli that have been paired with a highly aversive event (e.g. electrical shock). The key feature of our model is that learning of these conditioned responses in the central nucleus of the amygdala is modulated by two separate processes, one from basolateral amygdala and signaling a positive prediction error, and one from the vmPFC, via the intercalated cells of the amygdala, and signaling a negative prediction error. In addition, we propose that hippocampal input to both vmPFC and basolateral amygdala is essential for contextual modulation of fear acquisition and extinction. The model is sufficient to account for a body of data from various animal fear conditioning paradigms, including acquisition, extinction, reacquisition, and context specificity effects. Consistent with studies on lesioned animals, our model shows that damage to the vmPFC impairs extinction, while damage to the hippocampus impairs extinction in a different context (e.g., a different conditioning chamber from that used in initial training in animal experiments). We also discuss model limitations and predictions, including the effects of number of training trials on fear conditioning.     

Evaluative conditioning without directly experienced pairings of the conditioned and the unconditioned stimuli

Evaluative conditioning (EC) is the valence change of a stimulus (conditioned stimulus, CS) that is due to the previous pairing with another stimulus (unconditioned stimulus, US). We investigated whether EC can occur also when the CS–US pairings are not experienced directly by the participant but are implied by other events that the participant encounters. In two experiments, positive USs were presented in some trials and negative USs in other trials. Afterwards, participants were given information from which it was possible to conclude that CSs were covertly present during these trials. Finally, the valence of these CSs was registered using both implicit (Implicit Association Test, affective priming) and explicit measures (valence ratings). In line with the assumption that EC effects can be based on CS–US pairings that are not directly experienced, the valence of the CSs changed in the direction of the US with which they were covertly paired. This effect was observed both on explicit and on implicit measures. We argue that several aspects of our results are in line with propositional models of EC and fit less well with association formation models.     

Conditioned Inhibition of Cyclophosphamide-Induced Taste Aversion

Rats in an experimental group received trials during which 1 flavor (saccharin) was always followed by cyclophosphamide, an immunosuppressive drug, but another (vanilla) was not. An unconditioned stimulus-only group served as a control. Flavor-preference tests revealed that conditioned excitation and conditioned inhibition occurred in the conditioned group subjects but not in the control group subjects. This demonstration suggests that a conditioned inhibitor might be used to modify conditioned and unconditioned immune system functions, for example, natural killer-cell activity.     

Socially mediated learning in male Betta splendens. III: Rapid acquisitions

In four experiments with male Siamese fighting fish, the classical conditioning of visual/spatial cues with elicitors of aggression was demonstrated. These studies show that this type of socially mediated learning is more rapidly conditioned than was previously known. One 15-min training session is adequate to condition a preference for those cues that had recently been paired with conspecific images. Finally, behavior occurring during acquisition, in the presence of aggression-eliciting cues, was uncorrelated with the magnitude of the learned preferences that were assayed during extinction tests and in the absence of social stimuli.     

Is There Savings for Pavlovian Fear Conditioning after Neurotoxic Basolateral Amygdala Lesions in Rats?

Considerable evidence indicates an important role for amygdaloid nuclei in both the acquisition and expression of Pavlovian fear conditioning. Recent reports from my laboratory have focused on the impact of neurotoxic lesions of the basolateral complex of the amygdala (BLA) on conditional freezing behavior in rats. In these studies, I have observed severe effects of posttraining BLA lesions on the expression of conditional freezing even after extensive presurgical overtraining (25-75 trials). Moreover, I have found no evidence for sparing of fear memory (i.e., savings) in these rats when I assess their rate of reacquisition relative to BLA rats receiving minimal training (1 trial). In these experiments, freezing behavior was assessed using a conventional time-sampling procedure and expressed as a response probability. Although this measure is well established in the literature, it is conceivable that it is not sensitive to spared memory in rats with BLA lesions. To address this issue, I present a more detailed analysis of freezing behavior that quantifies latency to freeze, the number of freezing bouts, the duration of freezing bouts, and the probability distribution of bout lengths. I also include control data from untrained (no-shock) rats. Consistent with my earlier reports, I find no evidence of savings of fear memory in rats with neurotoxic BLA lesions using several measures of freezing behavior. These results reiterate the conclusion that fear memory, as it is expressed in freezing behavior, requires neurons in the BLA.