Undernutrition by rearing in large litters delays the development of reflexive, locomotor, and memory processes in mice

In three experiments, the effects of early postnatal undernutrition on the ontogeny of several behavioral capacities of varying complexity were investigated in the mouse. Following birth, mouse pups in all experiments were reared in either "normally nourished" or "undernourished" conditions by maintaining litter sizes at 6 or 16, respectively. Experiments 1 and 2 examined the development of adultlike patterns of swimming behaviors and spontaneous locomotor activity, respectively, as a function of litter size. The maturation of both behavior patterns was delayed by about 2 days in the 16-litter mice. In Experiment 3, normally nourished and undernourished mice received 25 trials in a shock-escape T-maze at 9, 11, and 13 days of age, followed by similar retention tests 24 hr later. Although litter size had little effect upon correct turns at each age during training, mice reared in litters of six exhibited significant retention of prior training by 12 days of age, whereas comparable retention was not noted for the large litter mice until 14 days of age. Overall, these results suggest that nutritional deficits, imposed by rearing in large litters during the postnatal period of rapid central nervous system maturation, retard the development of behavioral capacities involving both unlearned and learned responses.     

Aversiveness of denatonium saccharide and quinine in grasshopper mice Onychomys leukogaster

The responses toward denatonium saccharide and quinine by three rodent species differ from those exhibited by humans. This study measured the relative aversiveness of these two compounds in grasshopper mice (Onychomys leucogaster) to determine if this species responded similarly to or differently from these other rodents. In a choice test, the mice clearly preferred quinine over denatonium saccharide at concentrations of 1/10,000 and 1/50,000, but only marginally preferred quinine at a concentration of 1/1000. When denatonium or quinine was paired with toxicosis, both suppressed drinking at concentrations from 1/10,000 to 1/50,000, but only denatonium suppressed drinking at 1/100,000. Neither compound suppressed drinking at 1 part in million. Grasshopper mice perceived denatonium saccharide as more aversive than quinine in both experiments. Such a response resembled the behavior of humans more than that of the other three rodents previously tested.     

Development of the auditory orientation response in the albino rat (Rattus norvegicus)

The development of head orientation to auditory stimulation was examined in rat pups at Postnatal Days 8, 11, 14, 17, and 20. The animals were tested in a quiet environment with single bursts of 65 dB (SPL) broad-band noise. A reflexive head turn toward the sound was first seen on Postnatal Day 14 and subsequently on Days 17 and 20. This result demonstrates that the onset of directional auditory responses occurred between Day 11 and Day 14. The role of binaural cues in early sound orientation was examined in 17-day-old pups with monaural ligation of the external meatus. These animals were unable to localize a sound source and consistently turned toward the side of the unligated ear regardless of the position of the stimulus. Thus binaural cues were shown to be important for head orientation to sound in early development. In a separate study, head orientation to high and low frequency tone pips was examined. Directional responses were first seen on Day 12 for a 16-kHz tone and Day 14 for a 2-kHz tone. These results indicate an earlier onset for orientation to high frequency sounds in the rat.     

Learned suppression of ingestion: role of discriminative stimuli, ingestive responses, and aversive tastes

Three experiments were designed to demonstrate that animals learn to suppress contact with aversive-tasting foods and fluids, and to investigate the behavioral mechanisms of this learning. In Experiment 1, domestic chicks (Gallus gallus) rapidly learned to suppress drinking during a visual stimulus (SQ) that signaled ingestion of a quinine solution but drank normally during a second visual stimulus (SW) that signaled water access. In Experiment 2, chicks in Group Con received oral infusions of quinine contingent upon drinking during SQ. Group Non received oral quinine infusions during SQ yoked to those of Group Con and noncontingent upon drinking. Only Group Con suppressed drinking during SQ. The third experiment investigated the contribution of the aversive taste and the postingestive effects into either the beak or the crop following drinking during SQ. Only the orally infused subjects suppressed drinking during SQ. These studies suggest that the relation between the drinking response and the aversive taste of quinine during SQ is crucial to the learned suppression of ingestion produced by the present procedures. The implications of these results for theories of food selection and Batesian mimicry are discussed.     

Response of male and female Siberian hamsters towards pups

The influence of sex, reproductive maturity, and parental experience on the behavior of Siberian hamsters (Phodopus sungorus sungorus) toward strange pups was examined in this study. Immature, mature, or parentally experienced male and female Siberian hamsters were presented with 3- to 8-day-old pups. We recorded pup carrying during the initial 10 min, nesting with pups after 8 or 14 h, and attacking pups during the test period. Among inexperienced animals, more mature males attacked pups than did immature males or mature females. Parental experience significantly decreased pup attacks by males and increased nesting with pups by both males and females. Repeated testing did not modify the responses to pups. We conclude that in Siberian hamsters both caretaking and aggressive responses to pups may be shown by immature and mature animals of both sexes. Parental experience resulted in increased caretaking by males and females and decreased aggressive responses by males.     

Differential endocannabinoid regulation of extinction in appetitive and aversive Barnes maze tasks

CB 1 receptor-compromised animals show profound deficits in extinguishing learned behavior from aversive conditioning tasks, but display normal extinction learning in appetitive operant tasks. However, it is difficult to discern whether the differential involvement of the endogenous cannabinoid system on extinction results from the hedonics or the required responses associated with the disparate tasks. Here, we report that the CB 1 receptor antagonist rimonabant disrupts extinction learning in an aversive, but not in an appetitive, Barnes maze conditioning task. Accordingly, these results provide compelling support for the hypothesis that the endogenous cannabinoid system plays a necessary role in the extinction of aversively motivated behaviors but is expendable for appetitively motivated behaviors.     

Developmental expression of defensive responses during exposure to conspecific adults in preweanling rats (Rattus norvegicus).

I examined preweanling rats' (Rattus norvegicus) expression of ultrasounds and secretion of ACTH when exposed to unfamiliar adult male rats or to their mothers. Pups at 7 days of age produced similar levels of ultrasonic vocalization near both unfamiliar males and mothers. However, these pups could discriminate familiar from unfamiliar adults because ACTH was significantly higher in pups near adult males than in those near mothers. At 14 days of age, pups avoided adult males but not their mothers; therefore, adult males represented a significant threat. Importantly, 14-day-old rats significantly reduced ultrasound production only when near adult males. Pups at 21 days of age no longer emitted ultrasounds when socially isolated or when near conspecific adults. In addition, 14- and 21-day-old rats produced similar elevated ACTH levels across stimulus conditions. Results show significant changes in preweanling rats' responses to conspecific adults.     

Teacher escape,avoidance, and countercontrol behaviors: Potential resoponses to disruptive and aggressive behaviors of students with severe behavior disorders

We develop hypothese based on the research literature regarding behavioral responses to aversive stimuli. Specifically, escape, avoidance, and countercontrol responses are presented as teacher behaviors which may occur in the presence of disruptive and aggressive behaviors (aversive stimuli) which, in part, characterize many students with severe behavior disorders (SBD). The potential for teacher escape, avoidance, and countercontrol responses to the detrimental for both teachers and students is presented, as well as suggestions for addressing aversive behaviors of students in ways to reduce the potential detrimental impact.     

Milk availability modulates weaning in the Norway rat (Rattus norvegicus)

Two experiments were conducted to investigate the role of milk availability in the development of independent feeding and drinking in the Norway rat pup. Beginning on Day 14 postnatally, pups were exposed to different levels of milk supply by changing litter size from 8 to 4 versus 12 pups (Experiment 1) or limiting temporally the pups' access to a lactating dam to 8, 14, or 24 hr daily (Experiment 2). Both manipulations accelerated weaning in milk-poor pups in comparison with same-age pups with relatively greater milk supplies. By adding solid food and water to their diet, early weaning pups compensated for the negative energy consequences of milk reduction and achieved premanipulation growth rates. Milk availability thus appears to affect weaning, and it is suggested that the developmental changes in the nutritive energy balance between mother and offspring contribute to the emergence of independent ingestion.     

Behavioral responses of juvenile rats (Rattus norvegicus) to neonates after infusion of maternal blood plasma

Individual 18- or 30-day-old male and female Wistar rats (juveniles) were continuously exposed to 3-8-day-old pups for 5 days (sensitization) after intravenous (iv) infusion of maternal blood plasma (PL group) or 5% dextrose and water (IC group) through chronically implanted cannulas and were compared with nonhandled littermate controls (NHC group). The results showed complex interactions with sex and age of the animals tested, depending upon which maternal behaviors were examined. First, plasma from parturient females selectively increased retrieving behavior in 30-day-olds, and it was more powerful in females than in males. Second, on the first day, prior to sensitization, both PL and IC 30-day-olds showed higher frequencies of retrieving, crouching, anogenital licking, and contact than did nonhandled juveniles. Third, 30-day-olds that received maternal blood plasma continued to retrieve pups, with a latency peak for retrieving occurring at 72 hours, suggesting a long-term effect of plasma not seen in control animals. Fourth, 18-day-old subjects did not generally show effects of any of our manipulations, but they did show more nest building and contact behaviors than did 30-day-old subjects. Last, we found that the iv cannulation and infusion procedures led to a persistent dissociation of retrieving behavior from play in older animals and an integration of retrieving with crouching and licking regardless of whether maternal plasma or control infusion was administered. Retrieving behavior was associated with play behaviors (charge and pounce) in younger juveniles and in older, nonhandled control animals irrespective of treatment. For these animals, no integration of retrieving occurred with other maternal behaviors.     

The use of an unpleasant sound as the unconditional stimulus in aversive Pavlovian conditioning experiments that involve children and adolescent participants

Ethical considerations can prohibit the use of traditional unconditional stimuli (USs), such as electric shocks or loud tones, when children or adolescents participate in aversive Pavlovian conditioning experiments. The present study evaluated whether an unpleasant sound provides a viable alternative. Fifteen boys and girls aged 13 to 17 years completed a differential Pavlovian conditioning procedure in which a conditional stimulus (CS) was followed by the sound of metal scraping on slate. Acquisition of conditioned responses was found in startle blink magnitude, expectancy judgments of the sound, and skin conductance responses. Extinction of conditioned responses was found in all measures when the CS was no longer followed by the unpleasant sound. Subjective ratings and skin conductance responses indicated that the sound was unpleasant because of its qualitative features, rather than its intensity. The results support the use of an unpleasant sound as a low-risk alternative to traditional USs in aversive Pavlovian conditioning experiments with children and adolescents.     

Rat gestation during space flight: Outcomes for dams and their offspring born after return to earth

Sprague-Dawley rats were studied to learn whether gestation in the near-zero gravity, high radiation environment of space impacts selected mammalian postnatal events. Ten rats spent days nine to twenty of pregnancy aboard the space shuttle orbiterAtlantis (STS-66). Their movement, was studied shortly after return to Earth; subsequently, several of their offspring were cross-fostered and examined through postnatal day 81 (P81) for whole body growth and somatic motor development. Values for the flight animals were compared to ground-based control groups. Relative to controls, the pregnant flight rats showed a marked paucity of locomotion during the first few hours after returning to Earth. There was greater likelihood of perinatal morbidity for the offspring of flight dams when compared to the control groups. Whole body weight of surviving offspring, averaged for each group separately, showed typical sigmoidal growth curves when plotted against postnatal age. The flight group for our study had a larger ratio of female to male pups, and that was sufficient to account for the lower average daily weight gained by the flight animals when compared to the control groups. Walking was universally achieved by P13 and preceded eye opening which was complete in all pups by P17. Thus, both of these developmental horizons were attained on schedule in the flight as well as the control rats. Characteristic changes were observed in hind limb step length and gait width as the pups grew. These patterns occurred at the same time in each group of rats. Therefore, prenatal space flight from days nine to twenty of gestation did not interfere with the establishment of normal patterns for hind paw placement during walking.     

Changes in learning about aversive nonreward accounts for ontogeny of paradoxical appetitive reward effects in the rat pup: a mathematical model (DMOD) integrates results

Baby rats do not show any paradoxical appetitive reward effects (e.g., faster extinction following partial than continuous reinforcement, contrast effects when large and small rewards are given) until they are at least 12-14 days old, but can learn to pattern when reward and nonreward are alternated (e.g., Amsel, 1986). These results have been puzzling, but are now successfully integrated by DMOD (Daly MODification of Rescorla and Wagner's [1972] mathematical model; Daly & Daly, 1982). It was assumed that young rats do not have the capacity to learn about aversive nonreward but slowly gain this ability between 12 and 26 days (1 parameter reflecting the rate of conditioning of aversive nonreward, beta 1 for Vav, is increased from 0 to .15 beginning at 12 days). This theoretical integration has implications for understanding behavioral and neurological development of altricial organisms, and effects of neurological damage and toxic substances.     

CER suppression, passive-avoidance learning, and stress-induced suppression of drinking in the Syracuse high- and low-avoidance strains of rats (Rattus norvegicus)

The Syracuse strains of Long-Evans rats were selectively bred for good (SHA) or poor (SLA) avoidance learning in a two-way shuttle box, which resulted in a phenotypic difference that is correlated with behavior patterns indicative of emotional reactivity, SLA animals showing evidence of greater emotional reactivity than SHA animals. The first three experiments examined conditioned suppression of bar pressing and compared paired and unpaired conditioned- and unconditioned-stimulus presentations to evaluate the influence of conditioning versus primary aversive stimulation on baseline responding. SLA animals acquired conditioned suppression faster than SHA animals and also showed greater suppression of baseline responding than SHA animals. In Experiment 4, SLA animals learned a passive-avoidance task faster than SHA animals. In Experiment 5, SLA animals showed greater stress-induced suppression of drinking a weak quinine solution than SHA animals. These data are consistent with the hypothesis that SLA animals are more emotionally reactive than SHA animals.     

A machine-level software program for the generation of aversive conditioning schedules using the KIM-1 microprocessor

A microprocessor system can be used both to control aversive conditioning (classical, signaled and Sidman avoidance, and conflict) experiments and to acquire behavioral data in multiple subjects at a fraction of the cost of solid state systems. The software described in this paper can be used to program tones and shocks and count responses, independently, in up to 12 animals simultaneously.     

Differential associative conditioning and olfactory discrimination in the spiny lobster Panulirus argus

A differential aversive associative conditioning paradigm was used to assess the ability of the spiny lobster Panulirus argus both to associatively learn not to respond to the odorant stimulus to which it was conditioned and to discriminate between odorants. The paradigm consisted of pairing an aversive stimulus (pseudopredator) with a conditioned chemical stimulus (shrimp mixture). Four artificial mixtures (crab, mullet, oyster, and shrimp), each at 0.05 and 0.5 mM, were presented to the animals prior to, during, and following conditioning to both concentrations of the shrimp mixture. Pre- vs postconditioning changes in three types of behavioral responses (and an index based on a composite of these three behaviors) were used as indicators of learned aversions. Olfactory discrimination abilities were determined by comparing the aversion to the conditioned mixture with the aversions to the three nonconditioned mixtures. A high degree of associative learning was attained after 10 pairings of the pseudopredator with the shrimp mixture over a period of 5 test days. According to the aversion index, animals conditioned to shrimp mixture perceived crab mixture as being more similar to shrimp mixture than were mullet and oyster mixtures, but all three nonconditioned mixtures were perceived as being significantly different from the shrimp mixture. These results are in concordance with results of a cluster analysis based on the mixture compositions, which indicates that shrimp and crab mixtures are compositionally similar, while mullet and oyster mixtures are compositionally distinct from the shrimp mixture.     

Effect of postweaning social experience on response of Siberian hamsters (Phodopus sungorus sungorus) toward young

Between 18 and 50 days of age, Siberian hamsters were housed either with same-sex littermates, opposite-sex littermates, opposite-sex littermates and parents, or opposite-sex littermates, parents, and a younger litter. When adults, these animals were presented with two 3-8-day-old pups for 8 hr, and their responses were recorded. Rearing conditions did not affect behavior of females. Males housed with female littermates in the absence of a younger litter showed fewer pup attacks and more nesting with pups than did males housed only with other males. Thus, housing with females in the early postweaning period may influence males' later (adult) responses toward pups. Only among hamsters housed with same-sex littermates did males and females differ in their response to pups, a result emphasizing that sex differences in behavior may depend on early social rearing.     

Development switch in neural circuitry underlying odor-malaise learning

Fetal and infant rats can learn to avoid odors paired with illness before development of brain areas supporting this learning in adults, suggesting an alternate learning circuit. Here we begin to document the transition from the infant to adult neural circuit underlying odor-malaise avoidance learning using LiCl (0.3 M; 1% of body weight, ip) and a 30-min peppermint-odor exposure. Conditioning groups included: Paired odor-LiCl, Paired odor-LiCl-Nursing, LiCl, and odor-saline. Results showed that Paired LiCl-odor conditioning induced a learned odor aversion in postnatal day (PN) 7, 12, and 23 pups. Odor-LiCl Paired Nursing induced a learned odor preference in PN7 and PN12 pups but blocked learning in PN23 pups. 14C 2-deoxyglucose (2-DG) autoradiography indicated enhanced olfactory bulb activity in PN7 and PN12 pups with odor preference and avoidance learning. The odor aversion in weanling aged (PN23) pups resulted in enhanced amygdala activity in Paired odor-LiCl pups, but not if they were nursing. Thus, the neural circuit supporting malaise-induced aversions changes over development, indicating that similar infant and adult-learned behaviors may have distinct neural circuits.     

Aversive conditioning in the rat: effects of a benzodiazepine and of an opioid agonist and antagonist on conditioned hypoalgesia and fear.

Hypoalgesia and fear co-occurred in rats trained on a heated floor and tested for their latencies to paw lick on that floor and to step down onto a nonheated floor. These responses were extinguished, suggesting a mediation by aversive conditioning processes. A benzodiazepine impaired the acquisition of aversive conditioning, but it did not attenuate the expression of conditioned hypoalgesia. The opioid agonist morphine also impaired acquisition across a range of drug doses and variations in hypoalgesic tolerance, whereas the opioid antagonist naloxone facilitated acquisition. The results are discussed in terms of the perceptual-defensive-recuperative (Fanselow, 1986) and working memory (Grau, 1987) models of the mechanisms for the co-occurrence of conditioned hypoalgesia and fear.