Early Pavlovian conditioning impairs later Pavlovian conditioning

Four experiments tested the effects in the rat of very early experience with stimuli to be used later for Pavlovian conditioning. Beginning on postnatal Day 12, prior to the development of substantial detection and effective perception of visual and auditory stimuli, rats were given five daily experiences with either lights or tones and a footshock known to be an effective unconditioned stimulus at these ages. Twenty-four hours after the last of these experiences, pairings of either the light or tone and the unconditioned stimulus were given with parameters established to yield a moderate degree of conditioning in untreated preweanlings (Experiment 1). Experiment 2 determined that early experience with paired or unpaired presentations of either the light or tone and the unconditioned stimulus resulted in a failure to condition to these same lights or tones on postnatal Day 17, although nontreated pups from the same litters conditioned quite effectively. Experiment 3 determined that this early conditioning experience with either paired or unpaired presentations of the lights or tones and the unconditioned stimulus yielded impaired conditioning on postnatal Day 17 in the alternative sensory modality as well, although again nontreated siblings conditioned quite effectively. Experiment 4 replicated the results of each of Experiments 2 and 3 and determined in addition that despite the impairment in conditioning that resulted from early paired or unpaired experience with the stimuli of conditioning, early experience with the individual stimuli of conditioning—with only the CS, the US, or the context—did not result in a similar impairment in conditioning. Although the results were unexpected, they may be understood in part in terms of intersensory competition during development, and there is precedent in the literature for similar interfering effects of early learning on later learning in a variety of species. © 1996 John Wiley & Sons, Inc.     

Long-term impact of early olfactory experience on later olfactory conditioning

This study examined the duration of the effect of early olfactory experience in rats by determining the ease of conditioning and then reconditioning to an early-experienced odor. Rat pups (experimental group) were exposed to aniseed odor sprayed on the mother's belly from day 1 to 20 after birth. A control group was exposed only to water. At the ages of 21 and 40 days all the rats (experimental and control) were tested for preference for the odor of aniseed. Starting from day 41 after birth they were conditioned in a Y-maze to approach the odor of aniseed for a reward. We then divided both groups into five subgroups each. Each subgroup was retrained to approach aniseed after 5, 6, 7, 8 or 9 months, and their speeds of reconditioning to the odor were compared. The results showed that all rats in the early exposed group had remembered the odor and did not require reconditioning, unlike those in the group that had not had the early olfactory conditioning. The effect of the early experience was still detectable at least 5 months after last exposure to the odor.     

Heart rate and somatomotor activity in rats during signalled escape and yoked classical conditioning

In the first of three studies, heart rate, movement, and EMG activity during signalled escape and regular classical conditioning were examined in unrestrained and restrained groups of rats. The direction of the HR CR was accelerative in the unrestrained groups and decelerative in the restrained groups, regardless of the presence or absence of the escape contingency. Both CRs were enhanced by the presence of directionally similar changes in movement to the CS. The decelerations of the restrained groups were correlated with decreases in movement and increases in EMG activity. Increasing the somatomotor activity associated with the US failed to modify the decelerative direction of the HR CRs of restrained rats in the second and third studies. It was suggested that HR CRs in rats may be accompaniments of naturally occurring defense behaviors such as freezing in restrained rats and aggression in unrestrained rats.     

Classical conditioning in the rat fetus: involvement of mu and kappa opioid systems in the conditioned response

When the Embryonic Day 20 (E20) rat fetus is given a conditioning trial involving a paired presentation of an artificial nipple (the conditioned stimulus; CS) with an intraoral infusion of milk (the unconditioned stimulus; US), it shows evidence of classical conditioning when again exposed to the CS during a test trial. Specifically, the fetus shows fewer oral grasp responses (the conditioned response; CR) when continuously presented with the artificial nipple. The present study further investigated this classically conditioned reduction in oral grasping. Separate experiments (a) examined the time course of the reduction in oral grasping (Experiment 1), (b) characterized the time course of mu opioid (Experiment 2) and kappa opioid (Experiment 3) involvement in the CR, and (c) described changes in fetal behavior (Experiment 4) associated with mu and kappa opioid effects on responding to the artificial nipple. The results are discussed in terms of opioid involvement in establishing and maintaining early suckling behavior.     

Lever pressing and passive avoidance conditioning in cats with lesions of nonspecific thalamic nuclei

It is generally accepted that motor conditioned responses (MCR) result from the activity of all systems: afferent, integrating and storage, as well as efferent. Based on the postulation that some of the nonspecific thalamic nuclei are part of the afferent system, we trained cats to press a lever (MCR) in 2 situations. In one, signalled by illumination of a small circular disc, each lever press was reinforced by 0.5 ml of milk. In the other (light off) the response was not reinforced (suppression of MCR). Electrolytic lesions were made in centralis medialis and medialis dorsalis nuclei and after 24 hr the response was tested daily for at least 21 sessions. We observed that the largest lesions abolished the responses for 4 days, but the animals recovered afterwards. Furthermore, once the animals had recovered, the rate of lever pressing increased during the suppression situation. The difference between the slopes of the graphs relating lever pressing rate and session for the lesioned animals of Group 2 (lesions in centralis medialis, medialis dorsalis, centralis centralis and paraventricularis nuclei) and those for the sham-operated animals was at the 0.08 level, while for Group 3 (lesions mainly in central medialis) it was at the 0.05 level. All the cats acquired a one trial passive avoidance conditioning. Hence, the necessary information for the maintenance of MCR courses through other structures; however, the increase in lever pressing rate in SMCR seems to indicate the existence of an inhibitory function in these lesioned nuclei, mainly in centralis medialis.     

A developmental comparison of trace and delay eyeblink conditioning in rats using matching interstimulus intervals

The effects of conditioning paradigm and interstimulus interval (ISI) were evaluated in this study of the development of associative learning in rats. The acquisition of classical eyeblink conditioning (EBC) was examined in two paradigms (trace vs. delay), with three different ISIs (short, medium, or long) at two ages (postnatal Days 21-23 or 29-31). These data provide the first parametric analysis of ISI in developing animals trained with trace EBC procedures. Further, by comparing trace and delay EBC, it was determined that when ISI is held constant, acquisition is similar for both conditioning paradigms regardless of developmental age. This suggests a similar ontogeny of associative processes for delay and trace EBC that relies on common neural substrates. However, conditioned response timing (onset and peak latencies) was affected by age and paradigm, suggesting that different neural mechanisms may play a role in timing delay versus trace conditioned responses.     

Early maternal rejection and later social anxiety in juvenile and adult Japanese macaques

This study investigated the relationships between early maternal style and subsequent juvenile and adult behavior of offspring in Japanese macaques (Macaca fuscata). Early maternal style had no effect on baseline behavior of offspring when adult. In contrast, early maternal style was correlated with the response of adult offspring to stressful social interactions, and particularly with their response to actual or potential aggression. Infants whose mothers encouraged more independence showing high rates of rejection were less fearful and did cope better with stressful situations when adult. Although based on correlational data, these results suggest that in macaques maternal rejection can promote offspring independence and the development of a less anxious personality.     

The development of fear learning and generalization in 8-13 year-olds

The current study examined developmental changes in fear learning and generalization in 40 healthy 8–13 year‐olds using an aversive conditioning paradigm adapted from Lau et al. [Lau et al. [2008] Journal of the American Academy of Child and Adolescent Psychiatry 47:94–102]. In this task, the conditioned stimuli (CS+/CS?) are two neutral female faces, and the unconditioned stimulus is a fearful, screaming face. The second phase of the study also included a generalization stimulus (GS): a 50% blend of the CS± faces. The eye‐blink startle reflex was utilized to measure defensive responding. Patterns of fear learning and generalization were qualified by child age. Older children demonstrated greater fear learning (i.e., larger startle during CS+ than CS?) than younger children. In addition, older children exhibited the typical pattern of generalization observed in adults, whereas younger children did not. Finally, fear learning also related to contingency awareness; only children who correctly identified the CS+ demonstrated fear‐potentiated startle to the CS+. Clinical implications and future directions are discussed. © 2011 Wiley Periodicals,Inc. Dev Psychobiol 54: 675–684, 2012.     

Enhanced c-Fos expression in superior colliculus,paraventricular thalamus and septum during learning of cue-reward association

Reward-mediated associative learning is important for recognizing the significance of environmental cues. Such learning involves convergence of multimodal sensory inputs with circuits involved in affective and memory processes. Dopamine-dependent plasticity in the striatum plays a pivotal role, but the wider circuits engaged in cue-reward association are poorly understood. To identify candidate structures that may be of particular interest for further detailed electrophysiological and functional analysis, we quantified c-Fos expression in a selection of brain structures. c-Fos is a well-known marker of cell activation with additional potential importance for synaptic plasticity. We compared c-Fos expression between animals exposed to 100 pairings of a novel conditioned stimulus with a subsequent reward, and control animals exposed to the same number of cues and rewards, but where the cues and rewards occurred at random with respect to each other. We found significant increases in c-Fos expression in the superior colliculus in the group exposed to cue-reward pairing. This is consistent with previous recordings in conscious animals, showing modulation of phasic visual responses of single collicular neurons depending on their association with reward. Further, the data also suggest the possibility that the thalamic paraventricular nucleus and septal nuclei may be selectively activated during cue-reward association learning. Little is known of the neurophysiological responses in these structures during such tasks, so the present results suggest they would be targets of interest for future single-neuron recording experiments, designed to confirm whether the neurons show learning-specific modulation.     

Classical conditioning in the rat fetus: temporal characteristics and behavioral correlates of the conditioned response

This study examined the temporal characteristics and behavioral correlates of the conditioned response (CR) following classical conditioning of the embryonic Day 20 (E20 rat fetus). The conditioning procedure involved pairing of an artificial nipple (the CS) with an infusion of milk (the US) to establish classical conditioning. The test for classical conditioning involved measurement of a stimulus-evoked facial wiping response in a classical conditioning test. Experiment 1 compared the effectiveness of one- and three-trial procedures to establish classical conditioning. Experiment 2, 3, and 4 described the time course for the CR following one- and three-trial conditioning procedures. Experiments 3b and 4b describe the behavioral responses to (a) presentation of the CS at the time of conditioning, (b) infusion of the milk US at the time of conditioning, and (c) reexposure to the CS before the test for classical conditioning. Experiments 5 and 6 exposed the fetus to manipulations that either increased or decreased stretching (a behavior found to be associated with the CR). The results are discussed in terms of the temporal characteristics and behavioral correlates of conditioned and unconditioned responses and their mediation by activity in endogenous mu and kappa opioid systems.     

Effects of prior experience with dehydration and water on the time course of dehydration-induced drinking in weanling rats

Although cellular dehydration increases oral responding and swallowing of orally infused water in rats as young as 2 days old, it is not until well after the time of weaning that dehydration stimulates immediate water-seeking and initiation of drinking in situations where the water source must be approached voluntarily. Recent work has shown that the goal-directed appetitive sequence for drinking-orienting, approaching, and initiating contact with water-matures much later than the more precocial oral licking and swallowing behaviors, and normally comes to be elicited by dehydration only after post-weaning experience with dry food. In the current experiments we evaluate some critical features of post-weaning experience with dehydration and drinking, and find that prior experience with initiating drinking while dehydrated, but not experience with dehydration nor water per se, alters the time course of water intake during a subsequent hydrational challenge. The effects of experience are manifested as an increased proportion of water consumed in the early portion of the test, rather than a general increase in total consumption. These findings are consistent with the interpretation that prior experience is necessary for the coordination of water-oriented appetitive behaviors that lead to the initiation and maintenance of drinking bouts, and provide further evidence for an associative learning account of the acquisition of dehydration-induced drinking.     

Developmental environment: variables important for later learning and changes in cholinergic activity

Environmental experience of developing rats was manipulated in two ways. These were (1) providing increments in amount of visual stimulation vs. increased variety of novelty of visual stimulation, and (2) informal experience vs. formal training in discriminating between the given stimuli. At the conclusion of the developmental treatment an index of performance change was obtained by testing discrimination learning on a Lashley Jumping Stand. Effects on the cholinergic system, specifically, acetylcholinesterase (AChE) and cholinesterase (ChE) activities, were also examined. Increments in variety of stimulation, but not increases in amount, were found to contribute significantly to observed differences in AChE and ChE activity and in learning performance. Formal training in addition to enriched informal experience added little to either the biochemical effects or to the observed improvement in performance on the relevant learning task.     

Cardiorespiratory regulation and activity patterns of rat pups studied with their mothers during the nursing cycle

Rat pups aged 10 to 19 days were implanted with chronic electrodes and recorded while freely moving in the litter situation, during nursing and throughout naturally occurring maternal absences. Heart rates were significantly higher in the mother's presence (p<.01) while respiratory rates and percent of time spent active were identical under the 2 conditions. Pups' inactive heart rates progressively increased during the 20 min of nursing, while no such time trends were evident in other measures. Inactive heart rates decreased significantly (p<.01) as a function of age; respiratory rates and activity during nursing showed similar trends. A histogram of number of periods of activity bursts of different durations while pups were nursing showed a preponderance of 1- to 5-sec bursts which were observed to be associated with active sucking and pawing movements. This pattern of short bursts of spontaneous activity was repeated almost identically when the mother was absent, although the behavior was qualitatively different. In a second experiment, increases in pups' body temperature of .2°C to 1.0°C were found to accompany active nursing. If such increases were imposed by an artificial heat source, heart rates of pups actually fell slightly. In a third study, heart rates were recorded from nursing mothers and found to be relatively unaffected by stimulation from the pups.     

Repeated exposures to gustatory stimuli produce habituation or positive contrast effects in perinatal rats

Adult rats exhibit a decrease in consummatory responses following repeated presentations of a taste (habituation) and an increase in consummatory responses if they experience an upward shift in the magnitude or intensity of a gustatory stimulus (e.g., sucrose or saccharin). These responses do not represent a direct sensorimotor reaction to a gustatory cue, but rather reflect a change in responding based on the memory of a previous taste. Here, we sought to determine if fetal rats could (like adults) adjust their orofacial motor responses based on a memory of recent gustatory experience. Embryonic Day 18 (E18) or Day 19 (E19) rat fetuses received oral lavage with either 0.15 or 0.30% saccharin (SAC). Subsequently, observations of orofacial movements (mouthing and licking) following oral lavage with 0.30% SAC were made 50 min later, 24 hr later, or on postnatal Day 3 (P3). Thus, some animals were in a "shifted" condition in which they first experienced a relatively low concentration of SAC and then a higher one while control rats ("nonshifted") received 0.30% SAC during both taste exposures. Fetuses exhibited evidence of both habituation (with repeated presentation of the 0.30% SAC) and positive contrast effects (PCEs) (following an upward shift in SAC concentration) when retested 50 min after their first exposure to SAC on E19. However, these animals did not exhibit PCEs 24 hr later or 5 days later (on P3). Contrast effects were not observed when the initial SAC exposure was on E18, and habituation responses were variable depending on the time interval between the taste presentations to these animals. Rats with a 5- to 6-day latency between the two taste presentations showed neither PCEs nor habituation. Our data indicate that PCEs and habituation effects emerge at different ages, and their demonstration is dependent upon the latency between the taste presentations.     

Development of open-field behavior in mice: Effects of age and experience

Offspring from each of two inbred strains of mice (BALB/cJ and C57BL/6J) and their reciprocal crosses were tested in an open-field apparatus at 10 ages, from 15 to 120 days. Cross-sectional and longitudinal analyses were performed to assess separately the effects of age and prior test experience on open-field activity and defecation. Increased activity was associated with increased age in both strains and their F₁ reciprocal hybrids; however, the magnitude of this effect was a function of the genotype. Defecation also increased initially in all groups as a function of age; but, at later ages, different groups exhibited rather dissimilar defecation patterns. Prior experience was found to decrease activity in the open field in inbred strains and their reciprocal hybrids. The effect of prior experience on defecation was more complex: Within the two inbred strains, prior experience had relatively little effect on the pattern of defecation; for the F₁ hybrids, however, prior experience led to a significant increase in defecation at most ages. It was suggested that the differential effect of test experience on open-field activity and defecation represents a separation of two components of open-field behavior, “exploration” and “emotionality.”